Supplemental Data
Advancing our understanding and capacity to engineer nature’s CO2
sequestering enzyme, Rubisco
Spencer M. Whitney, Robert L. Houtz and Hernan Alonso
Table S1. Catalytic properties for different Rubisco forms determined at 25°C. Values are
adjusted as described in (Tcherkez et al., 2006) or those published since 2007 or represent
unpublished data by S.M Whitney. n.m., not measured. Individual data points are shown in
Figure 4 as dashes.
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Organism
Cyanobacteria
Anabaena variabilis
Synechococcus 7002
Synechococcus 6301
Thermosynecococcus BP1
Green algae
Chlamydomonas reinhardtii
Euglena gracilis
C4 higher plants
Amaranthus edulis
Amaranthus hybridus
Cynodon dactylon
Flaveria australasica
Flaveria bidentis
Flaveria kochiana
Flaveria trinervia
Paspalum dilatatum
Sorghum bicolor
Zea mays
Zoysia japonica
C3 higher plants
Arabidopsis thaliana
Atriplex glabriuscula
Chenopodium alba
Flaveria cronquistii
Flaveria pringlei
Helianthus annuus
Limonium gibertii
Nicotiana tabacum
Oryza sativa
Spinacia oleracea
Triticum aestivum
Non-green algae
Cylindrotheca fusiformis
Cylindrotheca N1
Galdieria sulfuraria
Griffithsia monilis
Olisthodiscus
Phaeodactylum tricornutum
Porphyridium
Bacteria
Chromatium vinosum
Rhodospirillum rubrum
Riftia pachyptila symbiont
Archaea
Methanocococcus burtonii
Methanocococcus Jannaschii
Thermococcus kodakaraensis
Form of
Rubisco
vCO2
KmCO2
(µM)
SC/O
-1
(s )
I (green)
I (green)
I (green)
I (green)
n.m.
13.4
11.8
n.m.
n.m.
246
200
n.m.
43
52
42
51
(Badger, 1980)
(Andrews and Lorimer, 1985)
(Mueller-Cajar and Whitney, 2008)
Whitney, unpublished
I (green)
I (green)
2.1
n.m.
31
n.m.
61
54
(Genkov et al., 2010)
(Jordan and Ogren, 1981)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
4.1
3.8
3.7
3.8
4.2
3.7
4.4
3.4
5.4
4.1
4.1
18.2
16.0
21.0
22.0
20.2
22.7
17.9
19.9
30.0
21.2
18.5
77
82
89
77
76
77
77
88
70
75
84
(Kubien et al., 2008)
(Jordan and Ogren, 1981)
(Carmo-Silva et al., 2010)
(Kubien et al., 2008)
(Kubien et al., 2008)
(Kubien et al., 2008)
(Kubien et al., 2008)
(Carmo-Silva et al., 2010)
(Sage and Seemann, 1993)
(Kubien et al., 2008)
(Carmo-Silva et al., 2010)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
I (green)
3.2
n.m.
2.9
3.1
3.1
2.9
4.6
3.4
n.m.
3.2
2.7
14.4
n.m.
11.2
10.8
12.0
n.m.
8.2
11.0
n.m.
12.1
10.9
81
87
79
81
81
84
110
82
85
80
100
Whitney, unpublished
(Badger and Collatz, 1977)
(Kubien et al., 2008)
(Kubien et al., 2008)
(Kubien et al., 2008)
(Sharwood et al., 2008)
(Parry et al., 2007)
(Whitney et al., 1999)
(Kane et al., 1994)
(Kubien et al., 2008)
(Carmo-Silva et al., 2010)
I (red)
I (red)
I (red)
I (red)
I (red)
I (red)
I (red)
2.0
0.8
1.2
2.6
0.8
3.4
1.6
36.0
31.0
3.3
9.3
59.0
28.0
22.0
111
106
166
167
100
113
129
(Read and Tabita, 1994)
(Read and Tabita, 1994)
(Whitney et al., 2001)
(Whitney et al., 2001)
(Read and Tabita, 1994)
(Whitney et al., 2001)
(Read and Tabita, 1994)
II
II
II
6.7
7.3
1
37
67
240
41
12
9
(Jordan and Chollet, 1985)
(Morell et al., 1990)
(Robinson et al., 2003)
III
III
III
2
n.m.
0.3
130
n.m.
52
1.2
0.5
11
(Alonso et al., 2009)
(Watson et al., 1999)
(Yoshida et al., 2007)
2
Reference
Literature cited
Alonso H, Blayney MJ, Beck JL, Whitney SM (2009) Substrate-induced Assembly of
Methanococcoides burtonii D-Ribulose-1,5-bisphosphate Carboxylase/Oxygenase
Dimers into Decamers. J Biol Chem 284: 33876-33882
Andrews TJ, Lorimer GH (1985) Catalytic properties of a hybrid between cyanobacterial large
subunits and higher plant small subunits of ribulose bisphosphate carboxylaseoxygenase. J Biol Chem 260: 4632-4636
Badger MR (1980) Kinetic-properties of ribulose 1,5-bisphosphate carboxylase-oxygenase from
Anabaena variabilis. Arch Biochem Biophys 201: 247-254
Badger MR, Collatz GJ (1977) Studies on the kinetic mechanism of RuBP carboxylase and
oxygenase reactions, with particular reference to the effect of temperature on kinetic
papameters. Carnegie YB 76: 355-361
Carmo-Silva AE, Keys AJ, Andralojc PJ, Powers SJ, Arrabaca MC, Parry MAJ (2010)
Rubisco activities, properties, and regulation in three different C-4 grasses under drought.
J Exp Bot 61: 2355-2366
Genkov T, Meyer M, Griffiths H, Spreitzer RJ (2010) Functional Hybrid Rubisco Enzymes
with Plant Small Subunits and Algal Large Subunits ENGINEERED rbcS cDNA FOR
EXPRESSION IN CHLAMYDOMONAS. J Biol Chem 285: 19833-19841
Jordan DB, Chollet R (1985) Subunit dissociation and reconstitution of ribulose-1,5bisphosphate carboxylase from Chromatium vinosum. Arch Biochem Biophys 236: 487496
Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose bisphosphate
carboxylase/oxygenase. Nature 291: 513-515
Kane HJ, Viil J, Entsch B, Paul K, Morell MK, Andrews TJ (1994) An improved method for
measuring the CO2/O2 specificity of ribulosebisphosphate carboxylase-oxygenase. Aust J
Plant Physiol 21: 449-461
Kubien DS, Whitney SM, Moore PV, Jesson LK (2008) The biochemistry of Rubisco in
Flaveria. J Exp Bot 59: 1767-1777
Morell MK, Kane HJ, Andrews TJ (1990) Carboxylterminal deletion mutants of
ribulosebisphosphate carboxylase from Rhodospirillum rubrum. FEBS Lett 265: 41-45
Mueller-Cajar O, Whitney SM (2008) Evolving improved Synechococcus Rubisco functional
expression in Escherichia coli. Biochem J 414: 205-214
Parry MAJ, Madgwick PJ, Carvalho JFC, Andralojc PJ (2007) Prospects for increasing
photosynthesis by overcoming the limitations of Rubisco. J Ag Sci 145: 31-43
Read BA, Tabita FR (1994) High substrate specificity factor ribulose bisphosphate carboxylase
oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial
rubisco containing algal residue modifications. Arch Biochem Biophys 312: 210-218
Robinson JJ, Scott KM, Swanson ST, O'Leary MH, Horken K, Tabita FR, Cavanaugh CM
(2003) Kinetic isotope effect and characterization of form II Rubisco from the
chemoautotrophic endosymbionts of the hydrothermal vent tubeworm Riftia pachyptila.
Limnol and Oceanog 48: 48-54
Sage RF, Seemann JR (1993) Regulation of rribulose-1,5-bisphosphate carboxylase/oxygenase
activity in response to reduced light intensity in C4 plants. Plant Physiol. 102: 21-28
Sharwood RE, von Caemmerer S, Maliga P, Whitney SM (2008) The catalytic properties of
hybrid Rubisco comprising tobacco small and sunflower large subunits mirror the
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kinetically equivalent source Rubiscos and can support tobacco growth. Plant Physiol
146: 83-96
Tcherkez GGB, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused
substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly
optimized. Proc Nat Acad Sci 103: 7246-7251
Watson GM, Yu JP, Tabita FR (1999) Unusual ribulose 1,5-bisphosphate
carboxylase/oxygenase of anoxic Archaea. J Bacteriol 181: 1569-1575
Whitney SM, Baldet P, Hudson GS, Andrews TJ (2001) Form I Rubiscos from non-green
algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J 26:
535-547
Whitney SM, von Caemmerer S, Hudson GS, Andrews TJ (1999) Directed mutation of the
Rubisco large subunit of tobacco influences photorespiration and growth. Plant Physiol
121: 579-588
Yoshida S, Atomi H, Imanaka T (2007) Engineering of a type III rubisco from a
hyperthermophilic archaeon in order to enhance catalytic performance in mesophilic host
cells. Appl Environ Microbiol 73: 6254-6261
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