COBIOT 508 1–7

Available online at www.sciencedirect.com

12
3 What is the maximum efficiency with which photosynthesis
4
can convert solar energy into biomass?
Xin-Guang Zhu1,2, Stephen P Long1,2 and Donald R Ort1,2,3

5 58

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6 Photosynthesis is the source of our food and fiber. Increasing report, http://www.sc.doe.gov/bes/reports/abstracts.html#- 59
7 world population, economic development, and diminishing SEU_rpt.pdf). Despite its quantity, solar energy is dif- Q2 60

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8 land resources forecast that a doubling of productivity is critical fused, which places a premium in all sectors of production 61
9 in meeting agricultural demand before the end of this century. A and agriculture on the overall efficiency of photosynthetic 62
10 starting point for evaluating the global potential to meet this solar energy conversion. In this context it is not surprising 63
11 goal is establishing the maximum efficiency of photosynthetic that ‘application of the revolutionary advances in 64
12 solar energy conversion. The potential efficiency of each step biology and biotechnology to the design of plants and 65
13 of the photosynthetic process from light capture to organisms that are more efficient energy conversion 66

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14 carbohydrate synthesis is examined. This reveals the maximum machines’ was identified as a major solar energy research 67
15 conversion efficiency of solar energy to biomass is 4.6% for C3 goal for the coming decades (Basic Research Needs for 68
16 photosynthesis at 30 8C and today’s 380 ppm atmospheric Solar Energy Utilization, DOE Solar Energy Workshop 69
17 [CO2], but 6% for C4 photosynthesis. This advantage over C3 report, http://www.sc.doe.gov/bes/reports/abstracts.html#- 70
will disappear as atmospheric [CO2] nears 700 ppm. SEU_rpt.pdf). A key starting point for identifying and 71
18
19 Addresses evaluating biotechnology targets for improving photosyn- 72
20
21
22
1
Q1 Department of Plant Biology, Institute of Genomic Biology,
University of Illinois at Urbana Champaign, United States
2
Department of Crop Sciences, Institute of Genomic Biology,
ED thetic solar conversion efficiency is a critical re-examin-
ation of the maximum efficiency of photosynthetic solar
73
74
University of Illinois at Urbana Champaign, United States
energy conversion that could theoretically be achieved in 75
23
24 3
Photosynthesis Research Unit, Agricultural Research Service, United managed ecosystems. The purpose of the analysis under- 76
25 States Department of Agriculture, Urbana, IL 61801, United States taken here is to draw on the state-of-the art understanding 77
26 of the mechanism of plant photosynthesis to establish the
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78
27 Corresponding author: Ort, Donald R (d-ort@uiuc.edu)
theoretical limit on photosynthetic solar energy conversion 79
efficiency that improved agronomy, breeding, and biotech- 80
28
29 Current Opinion in Biotechnology 2008, 19:1–7 nology can hope to approach. 81
30
31 This review comes from a themed issue on
Photosynthetically active radiation in the
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82
32 Plant Biotechnology
33 Edited by Joe Chappell and Erich Grotewold solar spectrum 83
34 As photosynthesis uses different wavelengths of radiant 84
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35 energy with different efficiencies, the first step is to 85

36 define the average energy spectrum at the Earth’s surface. 86
0958-1669/$ – see front matter
37
Published by Elsevier Ltd. The relative radiant energy density of the solar spectrum 87
38
39 at the surface of Earth’s atmosphere is given by the 88
DOI 10.1016/j.copbio.2008.02.004 Planck’s radiation distribution formula:
40
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41 relative energy flux density per unit wavelength interval

42
Introduction l5
43 / (1)
44 The world population is projected to grow to 10 billion ehc=lkT s  1 89
90
45 before reaching a plateau in the later part of this century, where l is the wavelength (nm); Ts is the temperature at 91
46 and increasing economic prosperity of the developing the surface of the Sun, which is about 5800 K; c is the 92
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47 world is forecast to soon place even greater demands on speed of light (3  1017 nm s1); k is the Bolzmann’s 93
48 agricultural production than on population growth. With constant (1.38  1023 kg m2 s2 K1 or J K1); and h 94
49 very few prospects to sustainably expand the 1.5 billion ha is the Planck’s constant (6.626  1034 J s). Heteroatomic 95
50 of cropland currently under cultivation [1], a doubling of gas molecules in the Earth’s atmosphere (e.g. CO2, H2O, 96
51 productivity will be needed to meet the increasing demand methane, nitrous oxide, etc.) absorb radiant energy at 97
52 before the end of this century. Current photosynthesis specific infrared wavelengths. These gases absorb most 98
53 underlies the production of all of our food and fiber and strongly in the wavelength (l) ranges 900–950, 1100– 99
54 biomass-based biofuel is increasingly being viewed as a 1150, 1350–1450, 1800–1950 nm, while ozone and oxygen 100
55 source of renewable fuels. More solar energy reaches the remove much of the energy below 400 nm (Figure 1). 101
56 Earth’s surface every hour (4.3  1020 J) than is consumed Photons above 740 nm in wavelength contain insufficient 102
57 on the planet in a year (4.1  1020 J) (Basic Research Needs energy to drive higher plant photosynthesis. Based on the 103
58 for Solar Energy Utilization, DOE Solar Energy Workshop measured average solar spectrum at the Earth’s surface, 104

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 COBIOT 508 1–7

2 Plant Biotechnology

120
Figure 1 of these wavelengths (e.g. anthocyanins in the epidermis) 121
but the energy is not transferred to photosynthesis. This 122
inactive absorption, to the extent that it happens, would 123
further lower photosynthetic conversion efficiency [2]. 124

Energy loss in rapid relaxation of higher 125

excited states of chlorophyll

F
126
The energy of a photon is determined by hc/l, with the 127
result that the energy of a blue photon (400 nm) is 75% 128

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greater than that of a red photon (700 nm). However, 129
higher excited states of chlorophyll very rapidly relax and 130
photochemistry is driven in the photosynthetic reaction 131
center with the energy of a red photon regardless of the 132
wavelength that was originally absorbed. Therefore 133
photosynthesis is unable to store the additional energy 134

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of blue photons. For the surface solar spectrum in the 135
photosynthetically active range (400–740 nm) the average 136
energy per mole of photons is 205 kJ. The energy 137
required to drive a charge separation event in Photosys- 138
tem II (PSII) is approximately 176 kJ mol1 (equal to the 139
energy of a photon of wavelength 680 nm) or 140
ED 171 kJ mol1 (l = 700 nm) for Photosystem I (PSI).
Therefore the average energy loss between absorption
141
142
and charge-separation in the photosystems will be 143
approximately (205  (176 + 171)/2) kJ mol1; that is, a 144
minimum of 6.6% of the incident solar energy is lost 145
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irretrievably as heat because of relaxation of higher 146
excited states of chlorophyll (Figure 2). 147

The distributions of energy density (a) and photon flux density (b) of a Energy loss between the reaction center 148
solar spectrum, which represents the average spectrum for the 48 and carbohydrate synthesis 149
continuous states of the United States over a period of one year. The
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The size of this loss differs between C4 and C3 species 150

energy density distribution was obtained directly from American
Society for Testing and Materials (http://rredc.nrel.gov/solar/spectra/
because of different ATP requirements of the two photo- 151
am1.5/) [33,34]. The photon flux density at each wavelength was synthetic pathways. 152
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calculated based on the energy in the typical solar spectrum (a) and
the energy in each photon at that wavelength. The band between the C3 photosynthesis 153
two vertical red lines represents the photosynthetically active
Examination of the Calvin cycle shows that three ATP 154
radiation (400–740 nm).
and two NADPH are required to assimilate one molecule 155
of CO2 into carbohydrate and to regenerate one ribulose- 156
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104 1,5-bisphosphate (RuBP) to complete the cycle. In whole 157

105 the proportion of total solar energy within the photo- chain linear electron transport the absorption of four 158
106 synthetically active band (400–740) is 48.7%; that is 51.3% photons will reduce one molecule of NADPH while 159
107 of the incident solar energy is unavailable to higher plant translocating a maximum of six protons into the thylakoid 160
108 photosynthesis (Figures 1 and 2). lumen; two from water oxidation and four from plasto- 161
quinol oxidation by the cytochrome b6/f complex [3]. 162
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109 Energy loss by reflectance of Since two NADPH, and therefore the absorption of eight 163
110 photosynthetically active light photons, are required for the assimilation of one CO2 into 164
111 Owing primarily to the relatively weak absorbance of carbohydrate, a maximum of 12 protons are transported 165
112 chlorophyll in the green band, vegetation is not a perfect into the lumen for each CO2 assimilated. With 4 protons 166
113 absorber of photosynthetically active radiation (400– required for the synthesis of 1 ATP [4–6], the 12 protons 167
114 740 nm). This, of course, is why most plants are green transported would therefore be just sufficient to support 168
115 and not black and it therefore limits maximum intercep- the synthesis of the 3 ATP required to balance 2 NADPH 169
116 tion of 400–740 nm light to 90%, that is, 10% of photo- in the assimilation of one CO2. The eight moles of red 170
117 synthetically active radiation is reflected. This represents photons, the minimum required to convert 1 mol of CO2 171
118 a minimum loss of 4.9% of the total incident solar radi- to carbohydrate, represents 1388 kJ energy. One-sixth of a 172
119 ation by reflection (Figure 2). Some plants contain varying mole of glucose, that is, a 1C carbohydrate unit, contains 173
120 amounts of nonphotosynthetic pigments that absorb light 477 kJ energy. Therefore the minimum energy loss in 174

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 COBIOT 508 1–7

Maximum efficiency of photosynthesis Zhu, Long and Ort 3

Figure 2

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PR
ED
Minimum energy losses calculated for 1000 kJ of incident solar radiation, at each discrete step of the plant photosynthetic process from interception
Insert "of" of radiation to the formation stored chemical energy in biomass. Both C3 and C4 (NADP–Malic Enzyme type) photosynthesis are considered.
CT
Calculations assume a leaf temperature of 30 8C and an atmospheric [CO2] of 380 ppm. The theoretical maximal photosynthetic energy conversion
efficiency is 4.6% for C3 and 6% C4 plants, calculated based on the total initial solar energy and the final energy stored in biomass. The arrows
indicate the amount of energy losses at different processes.

174 199
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175 electron transport and synthesis of carbohydrate within two NADPH required to fix one CO2 is just sufficient to 200
176 the Calvin cycle, that is, between energy trapping at the generate the three ATP also required. In C4, requiring 201
177 reaction centers and carbohydrate production, is 1  (477/ two additional ATP, then even at maximum efficiency, 202
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178 1388); this amounts to a loss of 24.6% of the energy proton translocation resulting from the reduction of 203
179 contained in the original incident solar radiation NADPH in noncyclic electron transport will be 204
180 (Figure 2). Therefore, the maximal energy conversion inadequate. Cyclic electron transport returns electrons 205
181 efficiency (ec) of C3 photosynthesis, before photorespira- from PSI back to the cytochrome b6/f complex resulting in 206
182 tion and respiration is 12.6% (Figure 2). the translocation of two protons per photon into the 207
thylakoid lumen [9,10]. In order for the cyclic flow to
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208
183 C4 photosynthesis provide the additional 8 protons needed to synthesize the 209
184 For simplicity, among the three major C4 subtypes, we 2 additional ATP, absorption of 4 additional photons at 210
185 will consider only the NADP–Malic Enzyme (ME) sub- PSI for a minimum total of 12 will be required per CO2 211
186 type, which includes all the major C4 crops, such as assimilated in C4 photosynthesis. Following our reason- 212
187 maize, sorghum, and sugar cane, and is considered to ing above for C3 photosynthesis, the minimum energy 213
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188 be the most efficient [7]. Here, five ATP and two loss in electron transport and synthesis of carbohydrate in 214
189 NADPH are required to assimilate one CO2 since, in C4 photosynthesis, between reaction center primary 215
190 addition to the energy requirement of the Calvin cycle, photochemistry and carbohydrate production is 216
191 two additional ATP are required for the phosphorylation 1  (477/2052); this amounts to a loss of 28.7% of the 217
192 of pyruvate to phosphoenol pyruvate. In effect these two energy contained in the original incident solar radiation 218
193 extra ATP represent a light-energy driven pump, which (Figure 2). Therefore, the maximal energy conversion 219
194 transports CO2 from the outer mesophyll and concen- efficiency (ec) of C4 photosynthesis, prior to respiration, is 220
195 trates it at the site of Rubisco in the inner photosynthetic 8.5% (Figure 2). 221
196 bundle sheath. The 10-fold higher concentration of
197 CO2 around Rubisco in C4 leaves, eliminates, or mini- Energy loss because of photorespiration 222
198 mizes photorespiration [8]. In C3 photosynthesis, we have In all eukaryotes photosynthetic CO2 assimilation is via 223
199 shown that translocation of protons in the reduction of the Rubisco, which catalyzes both the carboxylation and 224

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4 Plant Biotechnology

224
225 oxygenation of RuBP. Each oxygenation results in the Figure 3
226 formation of one molecule of glycolate. Two molecules of
227 glycolate are metabolized through the C2 pathway releas-
228 ing one CO2 and forming one molecule of phosphogly-
229 cerate, which re-enters the Calvin cycle. This process
230 known as photorespiration lowers the efficiency of photo-
231 synthesis both in requiring ATP and reductive energy,

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232 and in releasing recently assimilated CO2 [11]. Oxygen-
233 ation is competitively inhibited by CO2, such that in C4

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234 plants the concentration of CO2 at Rubisco in bundle
235 sheath cells largely eliminates photorespiration. How-
236 ever, some oxygenation may occur releasing CO2 back
237 to the mesophyll where it will be re-fixed at the cost of
238 additional energy. Here we consider the maximum poten-
239 tial efficiency, that is, zero photorespiration in C4 species.

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240 To determine the energetic cost of photorespiration we
241 define the ratio of RuBP oxygenation to carboxylation as
242 F, and compute the amount of ATP associated with one
243 carboxylation and F oxygenation as 3 + 3.5F, where 3.5 The effects of temperature and [CO2] on energy conversion efficiencies
244 represents the net ATP use in the C2 pathway and the of C3 and C4 photosynthesis for the past, current, and future
atmospheric conditions. We used three CO2 concentrations, that is, 220,
245 Calvin cycle associated with one oxygenation event. 380, and 700 ppm, which correspond to the average [CO2] of the past
246
247
Therefore, the number of ATP per CO2 fixation is
(3 + 3.5F)/(1  0.5F) where 0.5 represents the fact that
ED 25 My [16,17], current, and projected for year 2100. The O2
concentration was as 21% in all cases. Temperature influences both the
248 one CO2 is released for every two oxygenations. The solubility of CO2 and O2 in solution as well as the specificity of Rubisco
to CO2 relative to O2, which together drive the decrease in energy
decrease in ec caused by photorespiration (dpr) is therefore:
conversion efficiency with increase in temperature.
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277
3ð1  0:5FÞ
d pr ¼ 1  (2) recent rise in [CO2] and may be eliminated, except at the 278
250
249
251 3 þ 3:5F highest temperatures, by the end of this century (Figure 3). 279
252
The ratio of oxygenations to carboxylations (F) is Energy loss due to respiration 280
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The energy losses so far computed have been derived 281

O
253
254 F¼ (3) from the known, well-understood and conserved mech- 282
Ct anisms of photosynthesis. By contrast there is no quan- 283
255
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256 The symbols O and C represent the intercellular O2 and titatively defined mechanism of linkage between 284
257 CO2 concentrations. t is the specificity factor of photosynthetic rate and mitochondrial respiration. This 285
258 Rubisco for CO2 where specificity is the ratio of the final loss (Figure 2) can therefore only be an estimate 286
259 probabilities of carboxylation to oxygenation. Speci- based on empirical measurements. Measured ratios of 287
260 ficity declines with an increase in temperature, as does respiratory CO2 loss as a fraction of photosynthetic CO2 288
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261 the solubility of CO2 relative to O2 [12]. As a result, the uptake for major crops vary from 30% to 60% [18,19]. It 289
262 loss in the efficiency caused by photorespiration has been shown that there is heritable variation in this 290
263 increases with temperature. The effect of temperature ratio within crop species, and selection for a lower ratio in 291
264 on t is calculated from the empirically derived the case of ryegrass (Lolium perenne) resulted apparently in 292
265 equations of Bernacchi et al. [13], which yield a t of higher yielding lines [20]. We assume 30% here as the 293
266 71 at 30 8C. Given this value of t, a [CO2] of 380 ppm minimum respiratory loss that might be achieved without 294
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267 and an [O2] of 21%, the maximal ec of C3 plants would otherwise adversely affecting plant growth. This 295
268 be decreased by 49% at 30 8C, equivalent to a loss of represents a loss of the original incident solar energy of 296
269 6.1% of the originally intercepted solar radiation (Figure 2). 1.9% (C3) and 2.5% (C4), with the result that the maxi- 297
270 Because this loss is dependent on both temperature and mum conversion efficiencies of solar radiation into bio- 298
271 atmospheric [CO2] (see [14]), Figure 3 shows how con- mass ec are 4.6% (C3) and 6.0% (C4) at 30 8C. 299
272 version efficiency varies from 15 to 45 8C and at different
273 [CO2] which represent the average of Pleistocene con- Closing the gap between theoretical and 300
274 ditions (220 ppm), current (380 ppm) and forecast levels achieved conversion efficiencies 301
275 for 2100 (700 ppm) [15,16]. These simulations show a very The highest solar energy conversion efficiency reported 302
276 strong advantage for C4 photosynthesis at the atmospheric for C3 crops is about 2.4% and about 3.7% for C4 crops 303
277 [CO2] that prevailed for most of the past 25 M years [17] across a full growing season based on solar radiation 304
(Figure 3). This advantage has been diminished by the intercepted by the leaf canopy [2,21–23]. Higher 305

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Maximum efficiency of photosynthesis Zhu, Long and Ort 5

305 352
306 short-term conversion efficiencies are observed for brief nevertheless threefold to fourfold larger than the average 353
307 periods during the life of a crop reaching 3.5% for C3 conversion efficiency attained for major crops in the U.S. 354
308 and 4.3% for C4 [2]. A major factor that lowers the [31]. This difference is largely because of unfavorable 355
309 conversion efficiency below this theoretical value even physical environments for plant growth and reveals oppor- 356
310 for healthy canopies under optimal conditions is insuf- tunities for biotechnological improvement of productivity 357
311 ficient capacity to utilize all radiation incident on a leaf. through understanding crop stress tolerance. 358
312 The result is that although photosynthesis increases

F
313 linearly with light at low radiant energy fluxes, above Raising the ceiling on the maximum 359
314 about one quarter of full sunlight, the increase in conversion efficiency 360

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315 photosynthesis with further increase in light diminishes Finally, are there realistic opportunities to raise the 361
316 and there will often be no further increase above about theoretical maximum conversion efficiency? For C3 362
317 half of full sunlight [24]. Efficiency can be further plants, defeating photorespiration is an obvious target. 363
318 lowered by the fact that excess energy will engage This may be achieved by converting C3 crops to C4 or by 364
319 photoprotective mechanisms which will further impair improving the specificity of Rubisco for CO2. Conver- 365
320 efficiency [25–27]. There are two potential solutions: sion of a C3 to C4 crop would theoretically raise the 366

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321 improved canopy architecture or/and increased photo- maximum solar energy conversion efficiency at 30 8C 367
322 synthetic capacity per unit leaf area. First, canopy from 4.6% to 6%. If Rubisco can be engineered to 368
323 architecture. If for example, the sun is overhead, then completely eliminate the oxygenation reaction, this 369
324 high leaf angles will distribute the light more evenly would raise efficiency to 8.8%. This increase above 370
325 through the canopy and could reduce the proportion of the theoretical efficiency for C4 photosynthesis is 371
326 leaves that become light saturated. This design can because no additional ATP is required for concentrating 372
327
328
increase photosynthetic efficiency by as much as 45%,
relative to a canopy made up of horizontal leaves [28].
ED CO2. At present no Rubisco that lacks oxygenation
capacity has been identified, indeed most evidence
373
374
329 Second, photosynthetic capacity of individual leaves. In suggests that increase in specificity is at the expense 375
330 C3 leaves metabolic flux analysis suggests control of of catalytic rate [16]. However, by engineering the E. coli 376
331 photosynthesis is shared between Rubisco and proteins glycolate catabolic pathway into Arabidopsis (Arabidopsis 377
thaliana) chloroplasts [32] NADH would be generated
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332 involved in the regeneration of RuBP; the cytochrome 378
333 b6/f complex and sedoheptulose-1:7-bisphosphatase are in the conversion of the oxygenation product, glycolate, 379
334 most frequently implicated, reviewed in [29]. However, to phosphoglycerate rather than reduced ferredoxin con- 380
335 Rubisco already accounts for about 50% of leaf soluble sumed as in normal higher plant photorespiratory metab- 381
336 protein and it is first, doubtful that more protein could olism. This pathway also uses only half the ATP of the 382
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337 be added to chloroplasts of a healthy mature leaf higher plant pathway, and serves to concentrate CO2 at 383
338 and second, undesirable in modern agriculture to increase Rubisco. Based on the lower apparent CO2 compen- 384
339 nitrogen fertilizer requirements. Zhu et al. [30] built a sation points in the absence of mitochondrial respiration 385
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340 metabolic model of the photosynthetic carbon metabolism of the transformed plants [32], we computed that these 386
341 which described and linked every enzyme-catalyzed step transformed plants would have 14% more CO2 at 387
342 of the Calvin cycle, C2 pathway, and starch and sucrose Rubisco in the light. Taking this and the halving of 388
343 synthesis in the leaf. Using an evolutionary algorithm they the ATP requirement into account, if this introduction 389
344 showed that by substantial rearrangement in the invest- were completely successful in bypassing the normal 390
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345 ment of nitrogen among the proteins a 60% increase in photorespiratory pathway through the mitochondria 391
346 photosynthetic capacity might be achieved without any and peroxisomes, it would raise the maximum efficiency 392
347 increase in the total nitrogen invested into the photosyn- in C3 plants from the 4.6% of Figure 2 to 5.2% at 30 8C. If 393
348 thetic apparatus as a whole. the plants are able to take advantage of the NADH 394
349 generated in the chloroplast by the introduced E. coli 395
350 These observed solar energy conversion efficiencies glycolate catabolic pathway (e.g. production of ATP via a 396
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351 noted above for C3 and C4 crops, while well below the chloroplast/mitochondria shuttle) even greater improve- 397
352 theoretical maximums that we computed in Figure 2, are ment of the efficiency might be possible. 398

Appendix:. List of abbreviations. Values in parenthesis are those used in the analysis

Term Units Definition

c nm s1 Speed of light (3  1017)
CO2 mmol mol1 Atmospheric CO2 concentration (380)
C mmol mol1 Intercellular CO2 concentration (266)
dpr – Decrease in ec caused by photorespiration

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Appendix (Continued )
Term Units Definition
h Js Planck’s constant (6.626  1034)
I mmol m2 s1 Photon flux density
k J K1 Bolzmann’s constant (1.38  1023)
kcc s1 Number of carboxylation reactions per active site of Rubisco per second
koc s1 Number of oxygenation reactions per active site of Rubisco per second
Kmc mmol mol1 Rubisco Michaelis–Menten constant for CO2 (683 at 30 8C)

F
Kmo mmol mol1 Rubisco Michaelis–Menten constant for O2 (353 at 30 8C)
O2 mmol mol1 Atmospheric O2 concentration (210)
mmol mol1

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O Intercellular O2 concentration (210)
NAD-ME – NAD-Malic Enzyme subtype C4 photosynthesis
PSII – Photosystem II
Ts K Temperature at sun’s surface (5800)
F – The ratio of oxygenations to each carboxylation
t – The specificity of Rubisco for CO2 relative to O2 (91.3 at 25 8C)
l nm Wavelength
ec – Energy conversion efficiency

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398 444
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404
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491 27. Zhu X-G, Ort DR, Whitmarsh J, Long SP: The slow reversibility predicted 60% increase in photosynthetic capacity without any increase 512
492 of photosystem II thermal energy dissipation on transfer in the total N invested into the photosynthetic apparatus as a whole.
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501 photorespiratory pathway by converting glycolate to glycerate directly in 523

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502 30. Zhu X-G, de Sturler E, Long SP: Optimizing the distribution of the chloroplast. Although CO2 is still generated in this bypass pathway, the 524
503  resources between enzymes of carbon metabolism can release is in the direct vicinity of Rubisco thereby partially repressing 525
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Please cite this article in press as: Zhu X-G, et al., What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?, Curr Opin Biotechnol (2008),
doi:10.1016/j.copbio.2008.02.004