Substrate isomerization inhibits ribulosebisphospate carboxylase‐oxygenase during catalysis

Edmondson, Daryl L.; Kane, Heather J.; Andrews, T. John

doi:10.1016/0014-5793(90)80066-r

Cited by 95 publications

(68 citation statements)

References 19 publications

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“…For the spinach enzyme, this might be a result of inhibition caused by accumulating misprotonation by-products. Indeed, the kinetics of the decline for the spinach enzyme appeared quite reminiscent of the decline usually seen during catalysis which has been attributed to that cause (7)(8)(9)(10). Synechococcus Rubisco, however, is not subject to progressive inactivation during catalysis, at least at CO 2 saturation (16), and it showed a more pronounced decline such that, after 15-20 min, the rate of absorbance increase had fallen to approach the basal rate seen in the enzyme-free control.…”

Section: Conditions Leading To Exhaustion Of Gaseous Substrates-un-mentioning

confidence: 91%

“…Either spinach Rubisco has a larger fraction of its active sites occupied by the enediol under these conditions, as speculated by Morell et al (16), or it stabilizes or retains the enediol less effectively than Synechococcus Rubisco. An idea of the scale of deoxypentodiulose-P production can be obtained by comparing the amounts observed with those of xylulose-P 2 , previously shown to be produced by spinach Rubisco once in every 400 catalytic turnovers while a constant supply of CO 2 was maintained (10). In the present experiments, spinach Rubisco produced approximately two-thirds as much deoxypentodiulose-P as xylulose-P 2 , whereas for the Synechococcus enzyme the ratio was approximately one-fifth (Table II).…”

Section: ␤ Elimination Of the Enediol Intermediate Occurs Even Withmentioning

confidence: 99%

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Side Reactions Catalyzed by Ribulose-bisphosphate Carboxylase in the Presence and Absence of Small Subunits

Morell¹,

Wilkin²,

Kane

et al. 1997

Journal of Biological Chemistry

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The large subunit core of ribulose-bisphosphate carboxylase from Synechococcus PCC 6301 expressed in Escherichia coli in the absence of its small subunits retains a trace of carboxylase activity (about 1% of the k cat of the holoenzyme) ( the addition of CO 2 to ribulose-P 2 , producing two molecules of P-glycerate using a multistep reaction sequence involving at least three enzyme-bound catalytic intermediates (Scheme 1) (for reviews, see Refs. 1-3). Two of these intermediates, the first and the third, are strong nucleophiles by virtue of their enediol character. Both are susceptible to side reactions that abort the carboxylation sequence and compromise the catalytic efficiency of the enzyme. The first of these intermediates is the 2,3-enediol form of ribulose-P 2 produced by removal, by an enzymatic base, of the proton attached to C-3 of ribulose-P 2 . There may be two or more differently protonated forms of this intermediate; only the enediol form is shown in Scheme 1. Collectively, we refer to all forms of this intermediate as "the enediol." This is the species that must be attacked by CO 2 at C-2 and (concertedly or sequentially) by H 2 O at C-3 to form the six-carbon intermediate and thus allow carboxylation to proceed (Scheme 1). Three different classes of side reactions are known for this intermediate. First, the enediol is also attacked by O 2 at C-2, resulting in the formation of 2-phosphoglycolate which is, in turn, partially recycled to photosynthetic metabolism by the photorespiratory glycolate pathway (4 -6). Second, the enediol can be reprotonated incorrectly, producing pentulose bisphosphate isomers of the substrate (xylulose-P 2 and 3-ketoarabinitol-P 2 ) (7-12) which are strong inhibitors and/or very weak substrates of the enzyme (13-15). Third, mutants of Synechococcus PCC 6301 and Rhodospirillum rubrum Rubiscos were discovered that were compromised in their ability to stabilize the enediol. These mutant enzymes catalyzed the production of varying amounts of deoxypentodiulose-P as a result of ␤ elimination of the phosphoryl group attached to C-1 of the intermediate (P1) (16,17).The final intermediate in the carboxylation sequence is produced following cleavage of the C-2/C-3 bond of the six-carbon intermediate (Scheme 1). This aci-acid form of the P-glycerate molecule, derived from carbons 1 and 2 of ribulose-P 2 and the incoming CO 2 molecule, requires stereospecific protonation at C-2 to form P-glycerate. Only a single kind of side reaction is known for this intermediate, ␤ elimination of the phosphoryl moiety to produce enol-pyruvate and thus pyruvate (18). All wild-type Rubiscos studied so far partition approximately 0.7% of their aci-acid intermediate to pyruvate (18), and mutants are known in which this partitioning ratio is increased or decreased (14, 16, 17). Thus both of Rubisco's enediol-like intermediates are prone to ␤ elimination of the P1 phosphate group, * This work was supported by Australian National University's Center for Molecular Structure and Function. The costs of public...

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Section: Conditions Leading To Exhaustion Of Gaseous Substrates-un-mentioning

confidence: 91%

Section: ␤ Elimination Of the Enediol Intermediate Occurs Even Withmentioning

confidence: 99%

Side Reactions Catalyzed by Ribulose-bisphosphate Carboxylase in the Presence and Absence of Small Subunits

Morell¹,

Wilkin²,

Kane

et al. 1997

Journal of Biological Chemistry

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“…A curious difference between the Synechococcus and the spinach enzymes is that the latter displays "fallover" (7), the gradual loss of activity with time accompanied by production of XuBP in vitro. This phenomenon has not been detected in the Synechococcus enzyme (10). Given the very high degree of structural similarity of the XuBP complexes from spinach and Synechococcus (r.m.s.…”

Section: Xubp Binds As a Diol In The Active Site Of Spinach Rubisco-mentioning

confidence: 91%

“…Rubisco also catalyzes the epimerization of RuBP via the enediolate to xylulose 1,5-bisphosphate (XuBP, compound VII) as a result of incorrect stereochemical reprotonation of the enediol at C-3 (6 -9). If misprotonation is instead directed at C-2, 3-ketoarabinitol 1,5-bisphosphate (compound VIII) or 3-ketoribitol 1,5-bisphosphate may be produced (10,11). The epimerization products are all potent inhibitors of Rubisco.…”

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confidence: 99%

A Common Structural Basis for the Inhibition of Ribulose 1,5-Bisphosphate Carboxylase by 4-Carboxyarabinitol 1,5-Bisphosphate and Xylulose 1,5-Bisphosphate

Taylor

Fothergill²,

Andersson³

1996

Journal of Biological Chemistry

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“…regulators, such as RuBP (Jordan and Chollet, 1983), CAlP (Vu et al, 1984;Seemann et al, 1985;Servaites, 1990), and some by-products of the RuBP carboxylation reaction (Edmondson et al, 1990;Zhu and Jensen, 1991).…”

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confidence: 99%

Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Activase Deficiency Delays Senescence of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase but Progressively Impairs Its Catalysis during Tobacco Leaf Development

Caemmerer

Hudson

et al. 1997

Plant Physiology

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Transgenic tobacco (Nicofiana fabacum L. cv W38) plants with an antisense gene directed against the mRNA of ribulose-1,sbiphosphate carboxylase/oxygenase (Rubisco) activase grew more slowly than wild-type plants in a C0,-enriched atmosphere, but eventually attained the same height and number of leaves. Compared with the wild type, the anti-activase plants had reduced CO, assimilation rates, normal contents of chlorophyll and soluble leaf protein, and much higher Rubisco contents, particularly in older leaves. Activase deficiency greatly delayed the usual developmental decline in Rubisco content seen in wild-type leaves. This effect was much less obvious in another transgenic tobacco with an antisense gene directed against chloroplast-located glyceraldehyde-3-phosphate dehydrogenase, which also had reduced photosynthetic rates and delayed development. Although Rubisco carbamylation was reduced in the anti-activase plants, the reduction was not sufficient to explain the reduced photosynthetic rate of older antiactivase leaves. Instead, up to a 10-fold reduction in the catalytic turnover rate of carbamylated Rubisco in vivo appeared to be the main cause. Slower catalytic turnover by carbamylated Rubisco was particularly obvious in high-C0,-grown leaves but was also detectable in air-grown leaves. Rubisco activity measured immediately after rapid extraction of anti-activase leaves was not much less than that predicted from its degree of carbamylation, ruling out slow release of an inhibitor from carbamylated sites as a major cause of the phenomenon. Nor could substrate scarcity or product inhibition account for the impairment. We conclude that activase must have a role in vivo, direct or indirect, in promoting the activity of carbamylated Rubisco in addition to its role in promoting carbamylation.

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Substrate isomerization inhibits ribulosebisphospate carboxylase‐oxygenase during catalysis

Cited by 95 publications

References 19 publications

Side Reactions Catalyzed by Ribulose-bisphosphate Carboxylase in the Presence and Absence of Small Subunits

Side Reactions Catalyzed by Ribulose-bisphosphate Carboxylase in the Presence and Absence of Small Subunits

A Common Structural Basis for the Inhibition of Ribulose 1,5-Bisphosphate Carboxylase by 4-Carboxyarabinitol 1,5-Bisphosphate and Xylulose 1,5-Bisphosphate

Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Activase Deficiency Delays Senescence of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase but Progressively Impairs Its Catalysis during Tobacco Leaf Development

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