Photosynthesis involves capturing light energy and, most often, converting it to chemical energy stored as reduced carbon. It is the source of food, fuel, and fiber and there is a resurgent interest in basic research on photosynthesis. Plants make excellent use of visible light energy; leaves are ideally suited to optimize light use by having a large area per amount of material invested and also having leaf angles to optimize light utilization. It is thought that plants do not use green light but in fact they use green light better than blue light under some conditions. Leaves also have mechanisms to protect against excess light and how these work in a stochastic light environment is currently a very active area of current research. The speed at which photosynthesis can begin when leaves are first exposed to light and the speed of induction of protective mechanisms, as well as the speed at which protective mechanisms dissipate when light levels decline, have recently been explored. Research is also focused on reducing wasteful processes such as photorespiration, when oxygen instead of carbon dioxide is used. Some success has been reported in altering the path of carbon in photorespiration but on closer inspection there appears to be unforeseen effects contributing to the good news. The stoichiometry of interaction of light reactions with carbon metabolism is rigid and the time constants vary tremendously presenting large challenges to regulatory mechanisms. Regulatory mechanisms will be the topic of photosynthesis research for some time to come.

Introduction

Photosynthesis describes a broad array of processes by which light energy is captured and converted to chemical energy that is used in biological organisms. The energy is often stored on carbon as a change in oxidation state from +4 (carbon dioxide) to 0 (sugars). Bacteria, algae, and plants can carry out this process. However, in algae and plants the capacity for photosynthesis comes from a bacterial endosymbionts (chloroplasts) and so photosynthesis is primarily a bacterial process, although some archaea can also carry out photosynthesis. Photosynthesis is the source of nearly all carbon in the biosphere. Photosynthesis research has enjoyed a resurgence with government support supplemented by private foundations, especially for funding of the international RIPE project (Realizing Increased Photosynthetic Efficiency, https://ripe.illinois.edu/). Additional sources about emerging research in photosynthesis can be found in a recent special issue of The Plant Journal [1], which has a number of reviews on diffusion of CO2 through stomata and the mesophyll of leaves, among other topics. Also, more information can be had in any volume of the book series Advances in Photosynthesis and Respiration Including Bioenergy and Related Processes (https://www.springer.com/series/5599 See for example the latest volume, 45, covering algal research, [2]). Here I will offer descriptions and opinions on a subset of the current ‘hot topics' in plant photosynthesis research. There are many important emerging areas of research on photosynthesis in cyanobacteria not touched on here. One thread that runs through the topics in this paper is regulation of the many processes that constitute photosynthesis.

Light use

Which light?

Generally, photosynthesis makes use of what is called visible light, between 380 and 740 nm, between ultraviolet and infrared in the electromagnetic spectrum. The definition of photosynthetically active radiation (PAR) is more restricted, just 400 to 700 nm. Several pigments can be used for photosynthesis but by far the most common is chlorophyll. Chlorophyll extracted into a solvent has a relatively sharp peak of absorption in red light and a broader peak in blue light. Between is what is called the green gap although it turns out the gap is not that deep.

Plants use two different photosystems (PS I and PS II). The photosystems likely arose in different bacterial lineages and came together in cyanobacteria. The combined electron transport from PS II through a cytochrome b6/f complex to PS I allows conversion of light energy to reducing power (typically NADPH) and ATP simultaneously. Because there are different photosystems monochromatic light in the range of 680 to 700 nm is used inefficiently, but if light of wavelength less than 680 nm is combined with light of 700 nm then 700 nm light is more effective. This phenomenon is called the Emerson enhancement effect. Now, a similar argument has been made that light of wavelength longer than 700 nm can be used providing there is shorter wavelength light available simultaneously [3].

At the blue end of the spectrum it is known that light of wavelength shorter than 400 nm can drive photosynthesis. In Figure 5 of McCree [4], light of 350 nm was still 30% as effective as the maximum red light effectiveness. Most instruments designed to measure light available for photosynthesis cut on abruptly at 400 nm and off at 700 nm, both of which are oversimplifications of the true nature of PAR.

Most organisms use light throughout the visible spectrum much more uniformly than the strong red and blue absorption spectra of chlorophyll in a solvent would suggest. One reason is that chlorophylls are attached to proteins and exist in different environments, altering their absorption spectra. This makes both the red and blue peaks much broader, so much so that plants can use green light absorbed by chlorophyll. Cyanobacteria can fill in this green gap using specialized pigments called phycobilins (phycocyanin, allophycocyanin, and phycoerythrin). These pigments act as antennas and are arranged in protein structures called phycobilisomes that funnel green light to the photosystems.

Plants and algae do not have phycobilisomes even though, it is believed, chloroplasts were once free-living cyanobacteria. Nevertheless, plants make excellent use of green light, contrary to common thinking. In addition to the absorption band broadening described above, green light can have a much longer pathlength through a leaf than red or blue light. While red light and blue light will be absorbed quickly, sometimes only in the top layers of a leaf [5], green light can penetrate deeper into the leaf. Green light scattering will increase its pathlength and the chance for absorption by chlorophyll. This also causes backscattered light from a leaf to appear green. Under very bright light, red and blue light will be absorbed in the top layers of a leaf and excess red and blue photons will be dissipated there while green light penetrates to lower layers, where the chloroplasts are not saturated with light. This is why, under bright light, green light can be more effective than either red or blue light [6].

One way that plants do not fill the green gap is by carotenoid absorption acting as antennas for plant chlorophylls the way the phycobilisomes do for cyanobacteria. This common explanation, found in most biology textbooks, is simply wrong. Although blue light is more strongly absorbed than either green or red, it is less efficient per photon than either green or red light [4,7] (not just because of the extra energy per photon of blue light). This is because, rather than acting as antennas, the blue-absorbing carotenoids act as shades, absorbing light but not passing it to chlorophyll. Carotenoids are important for regulating energy flow and quenching dangerous side products formed by light absorption. Light energy can be efficiently passed from some carotenoids to chlorophylls in isolated reaction centers [8] but it has long been known that many carotenoids do not [9]. What is more, the absorption spectrum of carotenoids does not extend into the green very much further than chlorophyll absorption (Figure 1). Many carotenoids are not positioned to pass light energy to chlorophyll and so depress the efficiency of blue light. Even allowing for the stronger absorption of blue light, green light (e.g. 550 nm) can be more efficiently used for photosynthesis than blue light (e.g. 450 nm) in many situations (Figure 1).

Absorption of light by chlorophyll a and b, adsorption of light by leaves, and relative quantum efficiency as a function of wavelength.

Figure 1.
Absorption of light by chlorophyll a and b, adsorption of light by leaves, and relative quantum efficiency as a function of wavelength.

Chlorophyll a (dark green) and b (light green) and lutein (orange) (lutein is a highly abundant carotenoid in leaves) absorption spectra were determined for pigments separated by thin layer chromatography and dissolved in acetone. The adsorption of a typical leaf is shown by the gray line (right axis) and the relative quantum yield (left axis scale) is from data published by McCree [4]. Based on absorption spectra in solution, carotenoids do little to fill in the green gap, in plants this gap is mostly filled because of a long pathlength resulting from green light scattering.

Figure 1.
Absorption of light by chlorophyll a and b, adsorption of light by leaves, and relative quantum efficiency as a function of wavelength.

Chlorophyll a (dark green) and b (light green) and lutein (orange) (lutein is a highly abundant carotenoid in leaves) absorption spectra were determined for pigments separated by thin layer chromatography and dissolved in acetone. The adsorption of a typical leaf is shown by the gray line (right axis) and the relative quantum yield (left axis scale) is from data published by McCree [4]. Based on absorption spectra in solution, carotenoids do little to fill in the green gap, in plants this gap is mostly filled because of a long pathlength resulting from green light scattering.

Managing light energy in leaves

Light energy drives photosynthesis so the ability to capture light is crucial to the success of photosynthetic organisms. For plants this means efficient display of chlorophylls in leaves. Many leaves are very thin so that a maximal leaf area can be displayed for a given investment of resources. The specific leaf area (SLA, the area of leaves for a given leaf dry weight, or its inverse, leaf mass per area, LMA) is a major predictor of plant growth rate [10–13], often a better predictor than the rate of CO2 uptake per unit leaf area.

Specific leaf area will depend on leaf density, volume, and thickness [14]. Leaves can have variable volume of air space [15,16], too little airspace could reduce the diffusion of carbon dioxide while too much airspace could indicate an inefficient cellular architecture. There have been significant advances in understanding molecular signals that affect leaf cell morphology, providing a road map for improving leaf architecture to maximize photosynthesis [17,18].

Managing light energy in canopies

The canopy of trees can display a large number of leaves, but many lower leaves will be in the shade of higher leaves. This can also happen in crops. The amount of leaf area for a given ground area, called the leaf area index, can be as much as ten although three to five is more common. On the other hand, photosynthesis typically only makes use of about one quarter of full sunlight, i.e. photosynthetic rates are often [19] 75% of maximum by 500 µmol m−2 s−1 as has been published for field-grown soybeans [20] or leaves of oak trees exposed to full sun [21]. Many plants (for example Arabidopsis [22]) can respond to increasing light up to 500 µmol m−2 s−1 even when grown in just 100 µmol m−2 s−1. Light absorbed beyond 500 µmol m−2 s−1 is dissipated, essentially wasted. This can be useful if the light would otherwise go to competitors or deleterious if the light would otherwise go to lower leaves on the same plant. There have been attempts to improve crop yields by reducing the amount of chlorophyll in leaves so that upper leaves will be more transparent, allowing light to get to the lower leaves [20,23,24]. When chlorophyll is reduced uniformly through the canopy, the loss of photosynthesis in the top leaves was not fully compensated by the increased photosynthesis by the now better illuminated lower leaves. More work will be needed to distribute resources optimally through the canopy. Many plants have upper leaves displayed at many angles. The amount of light hitting a leaf will depend on the cosine of the angle between the rays of the sun and the surface of the leaf. Leaf angles at the tops of trees often approach a spherical distribution, that is the leaves could cover the various angles of a sphere. This allows light to penetrate into the canopy. This reduces the light intensity on the sun-exposed leaves but increases it for understory leaves. On the other hand, lower leaves can be arranged parallel to the ground so that whatever light does make it through the upper leaves will be maximally captured ([25,26] and unpublished data in Figure 2).

Leaf orientation and inclination.

Figure 2.
Leaf orientation and inclination.

Leaf inclination from horizontal and orientation around eight azimuth angles were measured at the top (Level A), mid canopy (Level B, LAI 1) and at the bottom of the canopy (Level C, LAI 3.3) of a white oak tree in the Duke Forest. The spread at level A indicates the leaves approximated a spherical distribution while at Level C the leaves were mostly parallel with the ground. The edge of the circle indicates an inclination of 90o from horizontal.

Figure 2.
Leaf orientation and inclination.

Leaf inclination from horizontal and orientation around eight azimuth angles were measured at the top (Level A), mid canopy (Level B, LAI 1) and at the bottom of the canopy (Level C, LAI 3.3) of a white oak tree in the Duke Forest. The spread at level A indicates the leaves approximated a spherical distribution while at Level C the leaves were mostly parallel with the ground. The edge of the circle indicates an inclination of 90o from horizontal.

Light: enough is enough

Most photosynthesis in leaves happens when there is considerably less light than is available in direct sunlight. This allows less investment in the enzymes needed for very rapid photosynthesis that could make use of full sunlight, allowing reduced SLA, which is associated with increased plant growth. However, this means that there will be occasions when there is more light than can be used in photosynthetic reactions. This can lead to photodamage. There are a number of mechanisms that allow photosynthetic organisms to protect themselves against excess light damage. Recent advances have been made in understanding the structure and function of the orange carotenoid protein (OCP) in cyanobacteria [27]. These proteins can move a carotenoid from one location to another within the protein and get attached to the phycobilisomes that harvest light. This causes the light energy to be harmlessly dissipated when it is in excess of what can be used by the photosystems [28–31].

In plants, which lack phycobilisomes, several methods are available for dissipating light energy, some safer than others. Many of these are assessed by analyzing chlorophyll fluorescence yields, especially in response to perturbations such as a flash of light five times brighter than full sunlight. The safest method for dissipating light energy is called energy-dependent quenching (qE) although the quenching here refers to the effect on chlorophyll fluorescence, not quenching of the incoming light energy. Following advice from W.W. Adams III I will reserve ‘quenching' for fluorescence and use the term dissipation for the fate of excess photons.

Energy-dependent quenching depends on energy in two ways [32,33]. First, light-driven electron transport causes an accumulation of protons in the lumen of the thylakoid. The lowered pH stimulates violaxanthin deepoxidase, which converts violaxanthin into zeaxanthin. The interconversion of violaxanthin and zeaxanthin is called the xanthophyll cycle. The presence of zeaxanthin potentiates qE. The second thing that has to happen is the low luminal pH that results in protonation of a PS II protein called PsbS [34]. Protonated PsbS in the presence of zeaxanthin causes changes in the light harvesting apparatus so that the energy of absorbed photons is dissipated as heat (radiationless decay) before it gets to PS II.

Current research focuses on the dynamics of regulation of photosynthetic electron and proton transport in a highly variable environment [35–37]. When the photon flux falling on a leaf increases abruptly, photosynthetic processes take a finite time to take full advantage [38]. In one study it was estimated that over 20% of potential photosynthesis was lost because of the need for induction of photosynthetic processes upon a shade to sun transition [39]. Mechanisms that dissipate excess light in bright light can be slow to reverse when a leaf is shaded. Speeding the relaxation of qE can increase overall plant yield [40,41].

Dissipation of light energy by qE develops and goes away more slowly than light can first exceed, and then become limiting again for photosynthesis. During the time between when light is in excess and when qE can safely dissipate the excess energy, photosynthesis can be damaged by the uncontrolled energy. Davis et al. [42] showed that the initial response to an abrupt increase in light is formation of the electrical component of the proton motive force and that this can lead to photodamage as a result of high speed light changes such caused by sunflecks [43].

If excess energy gets to PS II it can cause one of the proteins, D1, to be damaged. Fortunately, plants have an active repair cycle [44]. The PS II repair cycle and qE can both help plants cope with fluctuating light environments [45]. Photosynthetic electron flow from PS II to PS I can be slowed because of the energetic requirements for translocating protons at the cytochrome b6/f complex [46]. When electron transport is limited in this way electrons can build up on PS II, leading to damage. The buildup of electrons at PS II can be assessed by the chlorophyll fluorescence quenching parameter qL [47]. High qE and low qL will combine to protect PS I from overreduction. PS I overreduction may be more damaging than PS II overreduction because there is not a PS I repair mechanism like the PS II repair mechanism. Therefore, it is common to see evidence of excess light damage at PS II but rare to see damage at PS I, but when PS I is damaged it has more consequence for the plant than does PS II damage [48,49]. Plants lacking the proton gradient regulation 5 (PGR5) gene show no phenotype when grown under constant light but die under strongly fluctuating light because of damage to PS I [50].

Carbon

Rubisco: a complicated enzyme

Carbon dioxide is first fixed by the enzyme rubisco (C4 plants like corn and Crassulacean Acid Metabolism plants have chemical preconcentrating mechanisms but carbon dioxide first fixed by that mechanism is released for fixation by rubisco). There are many non-rubisco pathways for photosynthesis [51,52], especially among anaerobic bacteria; in terms of amount of carbon these are very minor but there have been many attempts to find more efficient engineered pathways of carbon fixation [51]. Improvements in rubisco have been attempted. In plants these are limited by the fact that the large subunit of rubisco is coded for in the chloroplast genome and transformation of the chloroplast genome is much more difficult than transformation of the nuclear genome. Nevertheless, significant advances in genetic engineering of plastids have been made [53–55].

Other ways to find improved rubisco relies on expressing it in bacteria [56] but this has been exceedingly difficult for the plant enzyme because it has not been possible to express it and have it fold properly in bacteria [57]. However, as a result of progress in understanding the chaperone proteins it has now been possible to express rubisco and all of the necessary chaperonins so that functional rubisco can be expressed in E. coli [58]. This opens the door to engineering to improve the catalytic properties of rubisco. Among the properties that need improvement is the kcat, which is between 2 and 10 s−1 per site [57]. This may be average when compared with all enzymes [59] but it is very slow for an enzyme in primary metabolism and as a result plants must invest vast amounts of nitrogen in the rubisco protein, significantly increasing the fertilizer costs of agriculture.

Another property of rubisco under current study is the need for post translational modification. A CO2 molecule (not the CO2 that will be fixed) is covalently bound to a lysine as a carbamate followed by addition of Mg2+ or Mn2+ (Figure 3) [60]. This is referred to as activation of rubisco and depends on an ATP-requiring AAA+ protein called rubisco activase [61], which removes molecules that bind slowly but tightly to rubisco [62,63]. There is some debate whether this is regulatory or represents a deficiency that could be corrected to engineer more efficient photosynthesis. Combining these two ideas, it could be that trapping of inactive rubisco by tight binding of inhibitors to the active site was a problem solved by activase but then activase evolved into a regulatory role. Cyanobacterial rubisco does not suffer as much from inactivation by tight binding inhibitors and yet many cyanobacteria have activase-like proteins that have a different function, possibly helping rubisco aggregate for inclusion in carboxysomes [64].

Rubisco (E) post-translational activation and the role of rubisco activase (Rca).

Figure 3.
Rubisco (E) post-translational activation and the role of rubisco activase (Rca).

Rubisco is carbamylated by CO2 and then a metal, usually magnesium, is added. This active form of the enzyme can bind ribulose 1,5-bisphosphate (RuBP) making the catalytically competent form ECMR. The carboxylation reaction releases ECM which can bind another RuBP. If RuBP binds before the enzyme is carbamylated it makes a dead-end complex. Although this reaction is slow, without activase free enzyme would accumulate as ER over time. Rubisco activase can remove RuBP to free up the enzyme, and then the faster carbamylation reaction will predominate. Other metabolites can bind tightly to different forms of rubisco and require rubisco activase to be released. Rubisco activase is regulated so that rubisco can be inactivated in low light, high CO2, or high temperature. E = free rubisco enzyme, R = RuBP bound to rubisco, C = carbamate of rubisco, M = metal on rubisco, normally Mg2+ but can be Mn2+, Rca = rubisco activase, PGA = 3-phosphoglyceric acid.

Figure 3.
Rubisco (E) post-translational activation and the role of rubisco activase (Rca).

Rubisco is carbamylated by CO2 and then a metal, usually magnesium, is added. This active form of the enzyme can bind ribulose 1,5-bisphosphate (RuBP) making the catalytically competent form ECMR. The carboxylation reaction releases ECM which can bind another RuBP. If RuBP binds before the enzyme is carbamylated it makes a dead-end complex. Although this reaction is slow, without activase free enzyme would accumulate as ER over time. Rubisco activase can remove RuBP to free up the enzyme, and then the faster carbamylation reaction will predominate. Other metabolites can bind tightly to different forms of rubisco and require rubisco activase to be released. Rubisco activase is regulated so that rubisco can be inactivated in low light, high CO2, or high temperature. E = free rubisco enzyme, R = RuBP bound to rubisco, C = carbamate of rubisco, M = metal on rubisco, normally Mg2+ but can be Mn2+, Rca = rubisco activase, PGA = 3-phosphoglyceric acid.

If regulation of rubisco activity by activase is not ideal for agricultural plants, or is no longer ideal in today's high CO2 atmosphere, then engineering activase could be an effective method for increasing crop yields. Rubisco activase is regulated by alternative splicing during gene expression [65], availability of ATP [66], redox [67], and phosphorylation [68]. Measurements show that rubisco is inactivated in low light [69], high CO2 [70], and high temperature [71,72]. While deactivation at low light or high CO2 can easily be ascribed to a regulatory adjustment of rubisco activity when it is in excess, the case for rubisco deactivation at high temperature being regulatory is less settled [71,73]. Significant advances have been made in finding [74,75] or engineering [76] thermostable forms of rubisco activase.

Rubisco makes mistakes

Rubisco catalysis is not completely specific for either substrates or products. For example, in addition to its primary product 3- phosphoglyceric acid [77], rubisco also makes a small amount of pyruvate [78]. This is slightly less efficient but provides a ready source of pyruvate for fatty acid synthesis and isoprenoid synthesis in chloroplasts. Rubisco will also use an alternative substrate, O2 instead of CO2 [79]. This reaction is not quite so harmless. One of the resulting molecules, 2-phosphoglycolate (2-PG), is a very potent inhibitor of the essential enzyme triose phosphate isomerase [80–82]. The reactions in plants that metabolize 2-PG are called photorespiration because they involve O2 uptake and CO2 release although instead of producing energetic molecules for the plant it consumes both ATP and reducing power, even more than when CO2 is fixed. Roughly speaking, for every three steps forward in CO2 fixation during photosynthesis, plants take one step backward in photorespiration [83,84]. Increasing CO2 decreases oxygenation and photorespiration but it will continue to be a major inefficiency of photosynthesis for a long time. The costs of photorespiration to agriculture is quite large [85].

Recent research aimed at developing methods to overcome the inefficiency of photorespiration has focused on alternative pathways for metabolizing 2-PG [86]. A major issue in photorespiratory metabolism is the release and refixation of ammonia. Ammonia fixation in the glutamine synthetase — glutamate oxoglutarate aminotransferase (GS-GOGAT) cycle for photorespiration greatly exceeds ammonia fixation needed for de novo protein synthesis. The nitrogen is used to make glycine and serine which are then metabolized eventually back to 3-phosphoglycerate to reenter the Calvin–Benson cycle. However, the glycine and serine can also be used directly for protein synthesis, in which case they can be seen as products of photosynthesis [87,88]. There are several ways in which photorespiratory metabolism has become intertwined with other metabolic pathways [89]. Bloom and Lancaster [90] propose that this provides an evolutionary pressure to regulate photorespiration at a significant rate, but the contrary view is that photorespiration is a ‘lemon' even if lemonade (improved nitrogen availability) was made. The frequent evolution of C4 plants [91] like corn, which have much reduced rates of photorespiration is typically invoked to indicate that plants can easily find mechanisms for nitrogen acquisition that do not depend on photorespiration.

A variety of alternative photorespiratory pathways have been engineered into plants. However, sometimes the pathway as proposed may not be what causes improved plant performance. An early, exciting report was made by Kebeish et al. [92]. They engineered a cyanobacterial pathway for glycolate metabolism consisting of a glycolate dehydrogenase (to make glyoxylate inside the chloroplast) followed by a glycolate carboligase (to make tartronic semialdehyde) and then tartronic semialdehyde reductase (to make glycerate). However, introducing the glycolate dehydrogenase alone caused a significant increase in photosynthetic rate [92,93]. In a similar vein, South et al. [94] reported that engineering glycolate dehydrogenase and malate synthase into tobacco (Figure 4) resulted in a stable transformant that performed better than the untransformed plant including under field conditions. This very encouraging finding suggests it will be possible to engineer more efficient photosynthesis. However, the mechanism is likely not precisely the pathway as drawn.

Alternative pathway number 3 to photorespiration of South et al. [94].

Figure 4.
Alternative pathway number 3 to photorespiration of South et al. [94].

Oxygenation of ribulose 1,5-bisphosphate yields one phosphoglycerate (PGA) and one 2-phosphoglycolate (2-PG). Dephosphorylation of 2-PG is critical. The engineered pathway involves glycolate dehydrogenase (GDH) using an unknown electron acceptor. Malate synthase (MS) combines acetyl CoA and glyoxylate to make malate. Malic enzyme (ME) action results in CO2, NADPH, and pyruvate. Pyruvate dehydrogenase (PDH) converts pyruvate to acetyl CoA releasing one CO2 but saving reducing power as NADH. See Fernie and Bauwe [86] for an expanded and more detailed look at alternative pathways for metabolizing 2-PG.

Figure 4.
Alternative pathway number 3 to photorespiration of South et al. [94].

Oxygenation of ribulose 1,5-bisphosphate yields one phosphoglycerate (PGA) and one 2-phosphoglycolate (2-PG). Dephosphorylation of 2-PG is critical. The engineered pathway involves glycolate dehydrogenase (GDH) using an unknown electron acceptor. Malate synthase (MS) combines acetyl CoA and glyoxylate to make malate. Malic enzyme (ME) action results in CO2, NADPH, and pyruvate. Pyruvate dehydrogenase (PDH) converts pyruvate to acetyl CoA releasing one CO2 but saving reducing power as NADH. See Fernie and Bauwe [86] for an expanded and more detailed look at alternative pathways for metabolizing 2-PG.

Gas exchange is often used to gain insight into photorespiration effects on net carbon assimilation. An important component of the equations found in many papers describing gas exchange measurements is the ratio of oxygenation to carboxylation 
vovc=Φ=1αΓC
1
where α is the proportion of CO2 molecules released per oxygenation, C is the partial pressure of CO2 at rubisco, and Γ* is called the rubisco compensation point and is where CO2 uptake equals CO2 release. The advantage of identifying Γ* is that it can be estimated experimentally and can be used in fitting models to gas exchange data although its measurement and meaning is not as straightforward as might be desired [95]. Several kinetic constants of rubisco are contained within Γ* 
Γ=αOkcatokcatcKcKo
2
Combining Eq. 1 and 2 
vovc=ααOCkcatokcatcKcKo
3
This shows that the amount of CO2 released per oxygenation cancels and so the ratio of vo/vcat any given ratio of O2 to CO2 is independent of α but Γ* is not. In the modified photorespiration pathways that involve glycolate metabolism to CO2 in the chloroplast, α changes from the usually accepted value of 0.5 to 2. Since the other components related to the kinetic constants of rubisco should not change, Γ* should increase by four-fold but in fact it was less in the plants with modified photorespiration [94]. Part of the explanation is that the 0.5 CO2 are released in the mitochondria while the CO2 released in the modified pathway is released inside the chloroplast, where it is more likely to be reassimilated. This could explain why the extra CO2 loss may not be as deleterious to photosynthetic rates as it would seem, but it cannot explain the decline in the estimation of Γ* at the rubisco compensation point where fluxes are slower and diffusional limitations less important.

Pathway 3 of South et al. (Figure 4) is energetically much more efficient than photorespiration (Table 1). The ATP requirement is reduced nearly to one half while the reducing power changes from a net loss to a net gain because of the loss of 2 CO2’s. These CO2’s would need to be refixed at a cost of NADPH and ATP. One way to analyze the energetics is a calculation of the ATP and NADPH that would be needed for the two pathways plus the energy needed to refix the lost CO2. This is shown in Table 1 as starting and ending with ribulose 5-phosphate. South's pathway 3 is more efficient in terms of reducing power than photorespiration if the reducing power at glycolate dehydrogenase can be recaptured, but photorespiration is more efficient than South's pathway 3 in terms of ATP. However, Pathway 3 requires many fewer steps and no diffusion from organelle to organelle. It is difficult to know the benefit of such a simplified system.

Table 1
Energetics of photorespiration and an alternative pathway
PathwayCO2ATPNADPH eq
Per oxygenation 
 Photorespiration −0.5 −3.5 −2 
 South pathway 3 −2 −2 +2 
Ru5P to Ru5P 
 Photorespiration −5.25 −3 
 South pathway 3 −8 −2 
PathwayCO2ATPNADPH eq
Per oxygenation 
 Photorespiration −0.5 −3.5 −2 
 South pathway 3 −2 −2 +2 
Ru5P to Ru5P 
 Photorespiration −5.25 −3 
 South pathway 3 −8 −2 

Costs are calculated per oxygenation or assuming additional CO2 fixation to compensate the carbon loss of each pathway. Negative sign indicates consumption or loss from the plant. The NADPH eq could be NADPH, NADH, or other unknown electron acceptors. The lower half presents estimates of costs that include refixation of released CO2, starting and finishing at ribulose 5-phosphate (Ru5P).

Finally, it is worth noting that the pathway shown in Figure 4 does not accommodate a role of photorespiration in N metabolism. The greater growth of plants with this pathway is evidence against the hypothesis that photorespiration is beneficial because of its role in nitrogen metabolism [90]

Determining why the genetic changes identified by South et al. increased photosynthesis and yield may lead to a better understanding of the regulation of photosynthesis and yield and allow even more targeted approaches to dealing with photorespiration. 2-PG was not measured but it may have been decreased by the introduction of the glycolate dehydrogenase, just as found by Nölke et al. [93]. Engineering photorespiration is likely to be of significant interest for the foreseeable future.

Carbon: active uptake

Most plants rely on diffusion for CO2 transport to rubisco. This saves energy but this kind of photosynthesis, called C3 photosynthesis, leaves plants vulnerable to photorespiration and would be difficult in aquatic situations where CO2 diffusion is very slow. Cyanobacteria have protein bounded microcompartments [96], of which the best known is the carboxysome, which contains all of the cell's rubisco. The carboxysome is part of a mechanism for active uptake of bicarbonate and conversion to CO2 at rubisco. Some researchers are trying to put carboxysomes into plants to overcome photorespiration and reduce the amount of rubisco needed for a given rate of photosynthesis [97]. There has also been significant interest in putting the C4 preconcentrating mechanism into C3 crops, especially into rice [98].

Regulation

Underlying many of the issues above is regulation. How are the various components of photosynthesis regulated so that everything works together harmoniously? This is a very important emerging research area in photosynthesis. A surprising finding was that photosynthesis could be divided between a state in which the capacity for regenerating the CO2 acceptor ribulose 1,5-bisphosphate (RuBP) is either (1) in excess and thus RuBP-saturated rubisco kinetics determined the CO2 response of photosynthesis or (2) limiting and so RuBP regeneration capacity determines the shape of the CO2 response of photosynthesis [99]. This either-or limitation is not intuitive for biologists but in fact is known to occur in many situations [100]. On the other hand, RuBP regeneration can be limited by either light availability and use or by the operation of the Calvin–Benson cycle. Increased capacity for Calvin–Benson cycle enzyme activity can lower the ΔG for ATP synthesis. This allows the lumen of the thylakoid to be regulated at a higher pH, reducing qE. This increases the efficiency of light use [101] so that when RuBP regeneration limits the photosynthetic rate, either light or Calvin–Benson cycle enzyme activity, or both simultaneously, may be rate setting factors.

Two other factors related to regulation of photosynthesis are important: (1) there is very little capacitance in the system, most carbon metabolite intermediates have pool sizes much <1 s (ie, would be consumed in under 1 s if production were abruptly halted, determined as flux divided by pool size), and (2) the stoichiometry is fixed, for example, the products of electron transport must be used in strict ratios. Excess ATP cannot compensate for a lack of NADPH (to a first approximation).

The stoichiometry issue is a very important area of current research into the regulation of photosynthetic processes. For example, C4 metabolism requires extra ATP but not NADPH (5 ATP/2 NADPH required) while the alternative, photorespiration, requires extra energy with only a slightly higher ATP/NADPH requirement (3.5 ATP/2 NADPH compared with 3 ATP/2 NADPH required in C3 photosynthesis). Current thinking is that normal linear electron flow produces 2.57 ATP per 2 NADPH because 14 protons are required for three ATPs in the ATP synthase [102]. This leaves an ATP deficit for the Calvin–Benson cycle and even more so when photorespiration is present. For example, if oxygenation happens at a rate or 0.3 times the rate of carboxylation then the required ratio would be 3.11 ATP per 2 NADPH for a deficit of 0.27 ATPs or 1.26 protons per one NADPH (or pair of electrons in linear electron flow). This ATP deficit can be made up by a number of mechanisms but the one most frequently discussed is cyclic electron flow involving PS I. Two pathways are normally discussed, one that involves NDH (NAD(P)H dehydrogenase) [103,104], which was thought to take electrons from NAD(P)H and recycle them back to the cytochrome b6/f complex while transporting as many as four protons per electron [104], which can then be used to make ATP. Recent evidence summarized by Peltier et al. [105] indicates that the true electron donor may be ferredoxin. The total activity of NDH may be limited and another cyclic electron flow pathway has been demonstrated. It has been thought to involve the PROTON GRADIENT REGULATION 5 protein (PGR5) and PGR5-like protein (PGRL1) and is sensitive to antimycin A [106]. The relative importance of these two pathways has been controversial, at least in part because the methods for measuring cyclic electron flow, especially in intact systems, are controversial. A recent report with C4 plants indicates that the NDH pathway may supply the cyclic electron flow for ATP synthesis while the PGR5 pathway contributes in some way to a sink for electrons downstream of PS I but does not contribute ATP [107]. Cyclic electron flow is also important in heat stress [108,109] and in a glucose-6-phosphate shunt [110]. Regulation of cyclic electron flow could involve sensing of ATP status [111].

Other methods for increasing ATP synthesis relative to NADPH include the water-water, or Asada, cycle in which electrons from water are eventually donated back to O2 to reform water. This pathway was also called pseudocyclic photophosphorylation. It is now mostly considered a method for detoxifying reactive oxygen species formed at PS I [112,113]. A second method involves export of reducing power from the chloroplast to the mitochondrion and making use of the mitochondrial electron transport chain to make ATP. This can be accomplished by the malate valve, export of malate and import of oxaloacetate can transfer NADH, or the non-phosphorylating glyceraldehyde 3-phosphate enzyme [114] that would allow GAP export and PGA import to the chloroplast transferring NADPH from the chloroplast to the cytosol [115,116].

Will increased photosynthesis increase crop yield?

As the source of reduced carbon for the plant it is almost axiomatic that improved photosynthesis will increase crop yield. The increased growth and yield of plants in elevated CO2 confirms the importance of photosynthesis. Nevertheless, some argue that improved photosynthesis alone is not the best way to improve crop yields [117]. To use a car analogy, it is important to pay attention to steering, tires, and even brakes on a race car, but a strong engine will be essential to a winning race team. It is important to understand the regulation of photosynthesis that integrates the chloroplast into the host metabolism. Research into regulation of photosynthesis to fit with the needs of the rest of the plant is in early stages and holds great promise for improving plant performance.

Summary

  • Fundamental pathways for electron and proton transport and carbon flow have been established; current research focuses on how these pathways are regulated.

  • Leaves take advantage of most of the visible light spectrum. Green light, rather than being mostly unused, is sometimes better used that blue light.

  • Regulation of light use is critical to take best advantage of available light while keeping deleterious light damage under control.

  • The speed of processes that adjust light use and CO2 use are currently being studied to optimize photosynthesis in highly variable environments.

  • The fixed stoichiometry of the various photosynthetic processes and extreme range of time constants make regulation essential. The importance of regulatory processes means that it can be hard to see past the regulation to observe the underlying constraints.

Competing Interests

The author declares that there are no competing interests associated with this manuscript.

Funding

Currently my research on photosynthesis comes from the US Department of Energy Award DE-FG02-91ER20021 and partial salary support is provided by Michigan AgBioResearch.

Author Contribution

T.D.S. wrote this review.

Abbreviations

     
  • 2-PG

    2-phosphoglycolate

  •  
  • NDH

    NAD(P)H dehydrogenase

  •  
  • PAR

    photosynthetically active radiation

  •  
  • PGR5

    proton gradient regulation 5

  •  
  • PS

    photosystems

  •  
  • RuBP

    ribulose 1,5-bisphosphate

  •  
  • SLA

    specific leaf area

References

References
1
Lawson
,
T.
and
Flexas
,
J.
(
2020
)
Fuelling life: recent advances in photosynthesis research
.
Plant J.
101
,
753
755
2
Larkum,
A.W.D.
,
Grossmann,
A.
and
Raven,
J
. (
2020
) Photosynthesis in Algae Biochemical and Physiological Mechanisms Cham Switzerland: Springer Nature Switzerland AG.
514
P,
3
Zhen
,
S.
and
Bugbee
,
B.
(
2020
)
Far-red photons have equivalent efficiency to traditional photosynthetic photons: implications for re-defining photosynthetically active radiation
.
Plant Cell Environ.
43
,
1259
1272
4
McCree
,
K.J.
(
1972
)
The action spectrum, absorptance and quantum yield of photosynthesis in crop plants
.
Agric. Meteor.
9
,
191
216
5
Slattery
,
R.A.
,
Grennan
,
A.K.
,
Sivaguru
,
M.
,
Sozzani
,
R.
and
Ort
,
D.R.
(
2016
)
Light sheet microscopy reveals more gradual light attenuation in light-green versus dark-green soybean leaves
.
J. Exp. Bot.
67
,
4697
4709
6
Terashima
,
I.
,
Fujita
,
T.
,
Inoue
,
T.
,
Chow
,
W.S.
and
Oguchi
,
R.
(
2009
)
Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green
.
Plant Cell Physiol.
50
,
684
697
7
Hogewoning
,
S.W.
,
Wientjes
,
E.
,
Douwstra
,
P.
,
Trouwborst
,
G.
,
Van Ieperen
,
W.
,
Croce
,
R.
et al (
2012
)
Photosynthetic quantum yield dynamics: from photosystems to leaves
.
Plant Cell
24
,
1921
1935
8
Croce
,
R.
,
Müller
,
M.G.
,
Bassi
,
R.
and
Holzwarth
,
A.R.
(
2001
)
Carotenoid-to-chlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorption measurements
.
Biophys. J.
80
,
901
915
9
Emerson
,
R.
and
Lewis
,
C.M.
(
1942
)
The photosynthetic efficiency of phycocyanin in chroococcus, and the problem of carotenoid participation in photosynthesis
.
J. Gen. Physiol.
25
,
579
10
Weraduwage
,
S.M.
,
Chen
,
J.
,
Anozie
,
F.C.
,
Morales
,
A.
,
Weise
,
S.E.
and
Sharkey
,
T.D.
(
2015
)
The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana
.
Front. Plant Sci.
6
,
167
11
John
,
G.P.
,
Scoffoni
,
C.
,
Buckley
,
T.N.
,
Villar
,
R.
,
Poorter
,
H.
and
Sack
,
L.
(
2017
)
The anatomical and compositional basis of leaf mass per area
.
Ecol. Lett.
20
,
412
425
12
Poorter
,
H.
,
Niinemets
,
Ü.
,
Ntagkas
,
N.
,
Siebenkäs
,
A.
,
Mäenpää
,
M.
,
Matsubara
,
S.
et al (
2019
)
A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance
.
New Phytol.
223
,
1073
1105
13
Lambers
,
H.
,
Chapin
, III,
F.S.
and
Pons
,
T.L.
(
2008
)
Plant Physiological Ecology
, 2nd edn,
Springer
, p.
604
14
Griffith
,
D.M.
,
Quigley
,
K.M.
and
Anderson
,
T.M.
(
2016
)
Leaf thickness controls variation in leaf mass per area (LMA) among grazing-adapted grasses in serengeti
.
Oecologia
181
,
1035
1040
15
Ren
,
T.
,
Weraduwage
,
S.M.
and
Sharkey
,
T.D.
(
2019
)
Prospects for enhancing leaf photosynthetic capacity by manipulating mesophyll cells morphology
.
J. Exp. Bot.
70
,
1153
1165
16
De La Riva
,
E.G.
Olmo
,
M.
,
Poorter
,
H.
,
Ubera
,
J.L.
and
Villar
,
R.
(
2016
)
Leaf Mass per Area (LMA) and its relationship with leaf structure and anatomy in 34 mediterranean woody species along a water availability gradient
.
PLoS ONE
11
,
e0148788
17
Weraduwage
,
S.M.
,
Kim
,
S.-J.
,
Renna
,
L.
,
Anozie
,
F.C.
,
Sharkey
,
T.D.
and
Brandizzi
,
F.
(
2016
)
Pectin methylesterification impacts the relationship between photosynthesis and plant growth
.
Plant Physiol.
171
,
833
848
18
Weraduwage,
S.M.
,
Campos,
M.L.
,
Yoshida,
Y.
,
Major,
I.T.
,
Kim,
Y.-S.
,
Kim,
S.-J.
et al (
2018
) Molecular mechanisms affecting cell wall properties and leaf architecture. In
The Leaf: A Platform for Performing Photosynthesis
(
Adams
,
W.W.
and
Terashima
,
I.
, eds), pp.
209
253
,
Springer International Publishing
,
Cham
19
Buckley
,
T.N.
and
Diaz-Espejo
,
A.
(
2015
)
Reporting estimates of maximum potential electron transport rate
.
New Phytol.
205
,
14
17
20
Slattery
,
R.A.
,
VanLoocke
,
A.
,
Bernacchi
,
C.J.
,
Zhu
,
X.-G.
and
Ort
,
D.R.
(
2017
)
Photosynthesis, light use efficiency, and yield of reduced-chlorophyll soybean mutants in field conditions
.
Front. Plant Sci.
8
,
549
21
Loreto
,
F.
and
Sharkey
,
T.D.
(
1990
)
A gas-exchange study of photosynthesis and isoprene emission in Quercus rubra L
.
Planta
182
,
523
531
22
Zuo
,
Z.
,
Weraduwage
,
S.M.
,
Lantz
,
A.T.
,
Sanchez
,
L.M.
,
Weise
,
S.E.
,
Wang
,
J.
et al (
2019
)
Expression of isoprene synthase in Arabidopsis alters plant growth and expression of key abiotic and biotic stress-related genes under unstressed conditions
.
Plant Physiol.
180
,
124
152
23
Ort
,
D.R.
and
Melis
,
A.
(
2011
)
Optimizing antenna size to maximize photosynthetic efficiency
.
Plant Physiol.
155
,
79
85
24
Walker
,
B.J.
,
Drewry
,
D.T.
,
Slattery
,
R.A.
,
VanLoocke
,
A.
,
Cho
,
Y.B.
and
Ort
,
D.R.
(
2018
)
Chlorophyll can be reduced in crop canopies with little penalty to photosynthesis
.
Plant Physiol.
176
,
1215
1232
25
Vicari
,
M.B.
,
Pisek
,
J.
and
Disney
,
M.
(
2019
)
New estimates of leaf angle distribution from terrestrial LiDAR: comparison with measured and modelled estimates from nine broadleaf tree species
.
Agric. For. Meteorol.
264
,
322
333
26
Liu
,
J.
,
Skidmore
,
A.K.
,
Wang
,
T.
,
Zhu
,
X.
,
Premier
,
J.
,
Heurich
,
M.
et al (
2019
)
Variation of leaf angle distribution quantified by terrestrial LiDAR in natural European beech forest
.
ISPRS J. Photogr. Rem. Sens.
148
,
208
220
27
Bao
,
H.
,
Melnicki
,
M.R.
and
Kerfeld
,
C.A.
(
2017
)
Structure and functions of orange carotenoid protein homologs in cyanobacteria
.
Curr. Opin. Plant Biol.
37
,
1
9
28
Dominguez-Martin
,
M.A.
and
Kerfeld
,
C.A.
(
2019
)
Engineering the orange carotenoid protein for applications in synthetic biology
.
Curr. Opin. Struct. Biol.
57
,
110
117
29
Kerfeld
,
C.A.
,
Melnicki
,
M.R.
,
Sutter
,
M.
and
Dominguez-Martin
,
M.A.
(
2017
)
Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs
.
New Phytol.
215
,
937
951
30
Muzzopappa
,
F.
and
Kirilovsky
,
D.
(
2020
)
Changing color for photoprotection: the orange carotenoid protein
.
Trends Plant Sci.
25
,
92
104
31
Kirilovsky
,
D.
and
Kerfeld
,
C.A.
(
2013
)
The orange carotenoid protein: a blue-green light photoactive protein
.
Photochem. Photobiol. Sci.
12
,
1135
1143
32
Ruban
,
A.V.
(
2016
)
Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage
.
Plant Physiol.
170
,
1903
1916
33
Zaks
,
J.
,
Amarnath
,
K.
,
Kramer
,
D.M.
,
Niyogi
,
K.K.
and
Fleming
,
G.R.
(
2012
)
A kinetic model of rapidly reversible nonphotochemical quenching
.
Proc. Natl Acad. Sci. U.S.A.
109
,
15757
15762
34
Li
,
X.P.
,
Gilmore
,
A.M.
,
Caffarri
,
S.
,
Bassi
,
R.
,
Golan
,
T.
,
Kramer
,
D.
et al (
2004
)
Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein
.
J. Biol. Chem.
279
,
22866
22874
35
Kramer
,
D.M.
,
Avenson
,
T.J.
and
Edwards
,
G.E.
(
2004
)
Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions
.
Trends Plant Sci
9
,
349
357
36
Li
,
J.
,
Tietz
,
S.
,
Cruz
,
J.A.
,
Strand
,
D.D.
,
Xu
,
Y.
,
Chen
,
J.
et al (
2018
)
Photometric screens identified Arabidopsis peroxisome proteins that impact photosynthesis under dynamic light conditions
.
Plant J.
97
,
460
474
37
Jeffrey A.
,
C.
,
Savage
,
L.J.
,
Zegarac
,
R.
,
Hall Christopher
,
C.
,
Satoh-Cruz
,
M.
,
Davis Geoffry
,
A.
et al (
2016
)
Dynamic environmental photosynthetic imaging reveals emergent phenotypes
.
Cell Syst.
2
,
365
377
38
Kalmatskaya
,
O.A.
,
Karavaev
,
V.A.
and
Tikhonov
,
A.N.
(
2019
)
Slow induction of chlorophyll a fluorescence excited by blue and red light in tradescantia leaves acclimated to high and low light
.
Photosyn. Res.
142
,
265
282
39
Taylor
,
S.H.
and
Long
,
S.P.
(
2017
)
Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity
.
Phil. Trans. Royal Soc. London B
372
,
20160543
40
Kromdijk
,
J.
,
Głowacka
,
K.
,
Leonelli
,
L.
,
Gabilly
,
S.T.
,
Iwai
,
M.
,
Niyogi
,
K.K.
et al (
2016
)
Improving photosynthesis and crop productivity by accelerating recovery from photoprotection
.
Science
354
,
857
861
41
Bennett
,
D.I.G.
,
Fleming
,
G.R.
and
Amarnath
,
K.
(
2018
)
Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting
.
Proc. Natl Acad. Sci. U.S.A.
115
,
E9523
E9531
42
Davis
,
G.A.
,
Kanazawa
,
A.
,
Schöttler
,
M.A.
,
Kohzuma
,
K.
,
Froehlich
,
J.E.
,
Rutherford
,
A.W.
et al (
2016
)
Limitations to photosynthesis by proton motive force-induced photosystem II photodamage
.
eLife
5
,
e16921
43
Way
,
D.A.
and
Pearcy
,
R.W.
(
2012
)
Sunflecks in trees and forests: from photosynthetic physiology to global change biology
.
Tree Physiol.
32
,
1066
1081
44
Theis
,
J.
and
Schroda
,
M.
(
2016
)
Revisiting the photosystem II repair cycle
.
Plant Sig. Behav.
11
,
e1218587
45
Townsend
,
A.J.
,
Ware
,
M.A.
and
Ruban
,
A.V.
(
2018
)
Dynamic interplay between photodamage and photoprotection in photosystem II
.
Plant Cell Environ.
41
,
1098
1112
46
Takizawa
,
K.
,
Cruz
,
J.A.
,
Kanazawa
,
A.
and
Kramer
,
D.M.
(
2007
)
The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf
.
Biochim. Biophys. Acta
1767
,
1233
1244
47
Kramer
,
D.M.
,
Johnson
,
G.
,
Kiirats
,
O.
and
Edwards
,
G.E.
(
2004
)
New fluorescence parameters for the determination of QA redox state and excitation energy fluxes
.
Photosyn. Res.
79
,
209
218
48
Tikkanen
,
M.
,
Mekala
,
N.R.
and
Aro
,
E.-M.
(
2014
)
Photosystem II photoinhibition-repair cycle protects photosystem I from irreversible damage
.
Biophys. Biochim. Acta
1837
,
210
215
49
Lima-Melo
,
Y.
,
Gollan
,
P.J.
,
Tikkanen
,
M.
,
Silveira
,
J.A.G.
and
Aro
,
E.-M.
(
2019
)
Consequences of photosystem I damage and repair on photosynthesis and carbon utilisation in Arabidopsis thaliana
.
Plant J.
97
,
1061
1072
50
Suorsa
,
M.
,
Jarvi
,
S.
,
Grieco
,
M.
,
Nurmi
,
M.
,
Pietrzykowska
,
M.
,
Rantala
,
M.
et al (
2012
)
PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions
.
Plant Cell
24
,
2934
2948
51
Bar-Even
,
A.
,
Noor
,
E.
,
Lewis
,
N.E.
and
Milo
,
R.
(
2010
)
Design and analysis of synthetic carbon fixation pathways
.
Proc. Natl Acad. Sci. U.S.A.
107
,
8889
8894
52
Bar-Even
,
A.
,
Noor
,
E.
and
Milo
,
R.
(
2012
)
A survey of carbon fixation pathways through a quantitative lens
.
J. Exp. Bot.
63
,
2325
2342
53
Whitney
,
S.M.
and
Andrews
,
T.J.
(
2001
)
Plastome-encoded bacterial ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) supports photosynthesis and growth in tobacco
.
Proc. Natl Acad. Sci. U.S.A.
98
,
14738
14743
54
Maliga
,
P.
(
2004
)
Plastid transformation in higher plants
.
Annu. Rev. Plant Biol.
55
,
289
313
55
Lin
,
M.T.
,
Occhialini
,
A.
,
Andralojc
,
P.J.
,
Parry
,
M.A.J.
and
Hanson
,
M.R.
(
2014
)
A faster Rubisco with potential to increase photosynthesis in crops
.
Nature
513
,
547
550
56
Mueller-Cajar
,
O.
and
Whitney
,
S.M.
(
2008
)
Evolving improved Synechococcus Rubisco functional expression in Escherichia coli
.
Biochem. J.
414
,
205
214
57
Bracher
,
A.
,
Whitney
,
S.M.
,
Hartl
,
F.U.
and
Hayer-Hartl
,
M.
(
2017
)
Biogenesis and metabolic maintenance of Rubisco
.
Annu. Rev. Plant Biol.
68
,
29
60
58
Aigner
,
H.
,
Wilson
,
R.H.
,
Bracher
,
A.
,
Calisse
,
L.
,
Bhat
,
J.Y.
,
Hartl
,
F.U.
et al (
2017
)
Plant RuBisCo assembly in E. coli with five chloroplast chaperones including BSD2
.
Science
358
,
1272
59
Bathellier
,
C.
,
Tcherkez
,
G.
,
Lorimer
,
G.H.
and
Farquhar
,
G.D.
(
2018
)
Rubisco is not really so bad
.
Plant Cell Environ.
41
,
705
716
60
Miziorko
,
H.M.
and
Lorimer
,
G.H.
(
1983
)
Ribulose-1,5-bisphosphate carboxylase/oxygenase
.
Annu. Rev. Biochem.
52
,
507
535
61
Portis
, Jr,
A.R.
(
2003
)
Rubisco Activase – Rubisco's catalytic chaperone
.
Photosyn. Res.
75
,
11
27
62
Mate
,
C.J.
,
Von Caemmerer
,
S.
,
Evans
,
J.R.
,
Hudson
,
G.S.
and
Andrews
,
T.J.
(
1996
)
The relationship between CO2-assimilation rate, Rubisco carbamylation and Rubisco activase content in activase-deficient transgenic tobacco suggests a simple model of activase action
.
Planta
198
,
604
613
63
Shivhare
,
D.
,
Ng
,
J.
,
Tsai
,
Y.-C.C.
and
Mueller-Cajar
,
O.
(
2019
)
Probing the rice Rubisco–Rubisco activase interaction via subunit heterooligomerization
.
Proc. Natl Acad. Sci. U.S.A.
116
,
24041
64
Lechno-Yossef
,
S.
,
Rohnke
,
B.A.
,
Belza
,
A.C.O.
,
Melnicki
,
M.R.
,
Montgomery
,
B.L.
and
Kerfeld
,
C.A.
(
2020
)
Cyanobacterial carboxysomes contain an unique rubisco-activase-like protein
.
New Phytol.
225
,
793
806
65
Werneke
,
J.M.
,
Chatfield
,
J.M.
and
Ogren
,
W.L.
(
1989
)
Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis
.
Plant Cell
1
,
815
825
66
Streusand
,
V.J.
and
Portis
, Jr,
A.R.
(
1987
)
Rubisco activase mediates ATP-dependent RuBPCase activation
.
Plant Physiol.
85
,
152
154
67
Zhang
,
N.
and
Portis
, Jr,
A.R.
(
1999
)
Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f
.
Proc. Natl Acad. Sci. U.S.A.
96
,
9438
9443
68
Kim
,
S.Y.
,
Harvey
,
C.M.
,
Giese
,
J.
,
Lassowskat
,
I.
,
Singh
,
V.
,
Cavanagh
,
A.P.
et al (
2019
)
In vivo evidence for a regulatory role of phosphorylation of Arabidopsis; Rubisco activase at the Thr78 site
.
Proc. Natl Acad. Sci. U.S.A.
116
,
18723
69
Mott
,
K.A.
,
Jensen
,
R.G.
,
O'Leary
,
J.W.
and
Berry
,
J.A.
(
1984
)
Photosynthesis and ribulose 1,5-bisphosphate concentrations in intact leaves of Xanthium strumarium L
.
Plant Physiol.
76
,
968
971
70
Sharkey
,
T.D.
,
Seemann
,
J.R.
and
Berry
,
J.A.
(
1986
)
Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to changing partial pressure of O2 and light in Phaseolus vulgaris
.
Plant Physiol.
81
,
788
791
71
Crafts-Brandner
,
S.J.
and
Salvucci
,
M.E.
(
2000
)
Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2
.
Proc. Natl Acad. Sci. U.S.A.
97
,
13430
13435
72
Feller
,
U.
,
Crafts-Brandner
,
S.J.
and
Salvucci
,
M.E.
(
1998
)
Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco
.
Plant Physiol.
116
,
539
546
73
Busch
,
F.A.
and
Sage
,
R.F.
(
2016
)
The sensitivity of photosynthesis to O2 and CO2 concentration identifies strong Rubisco control above the thermal optimum
.
New Phytol.
213
,
1036
1051
74
Shivhare
,
D.
and
Mueller-Cajar
,
O.
(
2017
)
In vitro characterization of thermostable CAM Rubisco activase reveals a Rubisco interacting surface loop
.
Plant Physiol.
174
,
1505
1516
75
Scafaro
,
A.P.
,
Bautsoens
,
N.
,
den Boer
,
B.
,
Van Rie
,
J.
and
Gallé
,
A.
(
2019
)
A conserved sequence from heat-adapted species improves rubisco activase thermostability in wheat
.
Plant Physiol.
181
,
43
76
Degen
,
G.E.
,
Worrall
,
D.
and
Carmo-Silva
,
E.
(
2020
)
An isoleucine residue acts as a thermal and regulatory switch in wheat Rubisco activase
.
Plant J.
in press
77
Sharkey
,
T.D.
(
2019
)
Discovery of the canonical Calvin–Benson cycle
.
Photosyn. Res.
140
,
235
252
78
Andrews
,
T.J.
and
Kane
,
H.J.
(
1991
)
Pyruvate is a by-product of catalysis by ribulosebisphosphate carboxylase/oxygenase
.
J. Biol. Chem.
266
,
9447
9452
PMID
[PubMed]
79
Bowes
,
G.
,
Ogren
,
W.L.
and
Hageman
,
R.H.
(
1971
)
Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase
.
Biochem. Biophys. Res. Comm.
45
,
716
722
80
Anderson
,
L.E.
(
1971
)
Chloroplast and cytoplasmic enzymes II. Pea leaf triose phosphate isomerases
.
Biochim. Biophys. Acta
235
,
237
244
81
Flügel
,
F.
,
Timm
,
S.
,
Arrivault
,
S.
,
Florian
,
A.
,
Stitt
,
M.
,
Fernie
,
A.R.
et al (
2017
)
The photorespiratory metabolite 2-phosphoglycolate regulates photosynthesis and starch accumulation in Arabidopsis
.
Plant Cell
29
,
2537
2551
82
Li
,
J.
,
Weraduwage
,
S.M.
,
Preiser
,
A.L.
,
Tietz
,
S.
,
Weise
,
S.E.
,
Strand
,
D.D.
et al (
2019
)
A cytosolic bypass and G6P shunt in plants lacking peroxisomal hydroxypyruvate reductase
.
Plant Physiol.
180
,
783
792
83
Sharkey
,
T.D.
(
1988
)
Estimating the rate of photorespiration in leaves
.
Physiol. Plant.
73
,
147
152
84
Busch
,
F.A.
(
2013
)
Current methods for estimating the rate of photorespiration in leaves
.
Plant Biol.
15
,
648
655
85
Walker
,
B.J.
,
VanLoocke
,
A.
,
Bernacchi
,
C.J.
and
Ort
,
D.R.
(
2016
)
The costs of photorespiration to food production now and in the future
.
Annu. Rev. Plant Biol.
67
,
107
129
86
Fernie
,
A.R.
and
Bauwe
,
H.
(
2020
)
Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway
.
Plant J.
102
,
666
677
87
Harley
,
P.C.
and
Sharkey
,
T.D.
(
1991
)
An improved model of C3 photosynthesis at high CO2: reversed O2 sensitivity explained by lack of glycerate reentry into the chloroplast
.
Photosyn. Res.
27
,
169
178
88
Busch
,
F.A.
,
Sage
,
R.F.
and
Farquhar
,
G.D.
(
2018
)
Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway
.
Nat. Plants
4
,
46
54
89
Busch
,
F.A.
(
2020
)
Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism
.
Plant J.
101
,
919
939
90
Bloom
,
A.J.
and
Lancaster
,
K.M.
(
2018
)
Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis
.
Nat. Plants
4
,
414
422
91
Sage
,
R.F.
and
Stata
,
M.
(
2015
)
Photosynthetic diversity meets biodiversity: the C4 plant example
.
J. Plant Physiol.
172
,
104
119
92
Kebeish
,
R.
,
Niessen
,
M.
,
Thiruveedhi
,
K.
,
Bari
,
R.
,
Hirsch
,
H.J.
,
Rosenkranz
,
R.
et al (
2007
)
Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana
.
Nat. Biotech.
25
,
593
599
93
Nölke
,
G.
,
Houdelet
,
M.
,
Kreuzaler
,
F.
,
Peterhänsel
,
C.
and
Schillberg
,
S.
(
2014
)
The expression of a recombinant glycolate dehydrogenase polyprotein in potato (Solanum tuberosum) plastids strongly enhances photosynthesis and tuber yield
.
Plant Biotech. J.
12
,
734
742
94
South
,
P.F.
,
Cavanagh
,
A.P.
,
Liu
,
H.W.
and
Ort
,
D.R.
(
2019
)
Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field
.
Science
363
,
eaat9077
95
Walker
,
B.J.
,
Orr
,
D.J.
,
Carmo-Silva
,
E.
,
Parry
,
M.A.J.
,
Bernacchi
,
C.J.
and
Ort
,
D.R.
(
2017
)
Uncertainty in measurements of the photorespiratory CO2 compensation point and its impact on models of leaf photosynthesis
.
Photosyn. Res.
132
,
245
255
96
Kirst
,
H.
and
Kerfeld
,
C.A.
(
2019
)
Bacterial microcompartments: catalysis-enhancing metabolic modules for next generation metabolic and biomedical engineering
.
BMC Biol.
17
,
79
97
Hanson
,
M.R.
,
Lin
,
M.T.
,
Carmo-Silva
,
A.E.
and
Parry
,
M.A.J.
(
2016
)
Towards engineering carboxysomes into C3 plants
.
Plant J.
87
,
38
50
98
Ermakova
,
M.
,
Danila
,
F.R.
,
Furbank
,
R.T.
and
von Caemmerer
,
S.
(
2020
)
On the road to C4 rice: advances and perspectives
.
Plant J.
101
,
940
950
99
Farquhar
,
G.D.
,
von Caemmerer
,
S.
and
Berry
,
J.A.
(
1980
)
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species
.
Planta
149
,
78
90
100
Koshland
,
D.E.
(
1987
)
Switches, thresholds and ultrasensitivity
.
Trends Biochem. Sci.
12
,
225
229
101
Simkin
,
A.J.
,
McAusland
,
L.
,
Headland
,
L.R.
,
Lawson
,
T.
and
Raines
,
C.A.
(
2015
)
Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco
.
J. Exp. Bot.
66
,
4075
4090
102
Hahn
,
A.
,
Vonck
,
J.
,
Mills
,
D.J.
,
Meier
,
T.
and
Kühlbrandt
,
W.
(
2018
)
Structure, mechanism, and regulation of the chloroplast ATP synthase
.
Science
360
,
eaat4318
103
Strand
,
D.D.
,
D'Andrea
,
L.
and
Bock
,
R.
(
2019
)
The plastid NAD(P)H dehydrogenase-like complex: structure, function and evolutionary dynamics
.
Biochem. J.
476
,
2743
2756
104
Strand
,
D.D.
,
Fisher
,
N.
and
Kramer
,
D.M.
(
2017
)
The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow
.
J. Biol. Chem.
292
,
11850
11860
105
Peltier
,
G.
,
Aro
,
E.-M.
and
Shikanai
,
T.
(
2016
)
NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis
.
Annu. Rev. Plant Biol.
67
,
55
80
106
Wang
,
C.
,
Takahashi
,
H.
and
Shikanai
,
T.
(
2018
)
PROTON GRADIENT REGULATION 5 contributes to ferredoxin-dependent cyclic phosphorylation in ruptured chloroplasts
.
Biophys. Biochim. Acta
1859
,
1173
1179
107
Tazoe
,
Y.
,
Ishikawa
,
N.
,
Shikanai
,
T.
,
Ishiyama
,
K.
,
Takagi
,
D.
,
Makino
,
A.
et al (
2020
)
Overproduction of PGR5 enhances the electron sink downstream of photosystem I in a C4 plant, Flaveria bidentis
.
Plant J.
in press
108
Zhang
,
R.
and
Sharkey
,
T.D.
(
2009
)
Photosynthetic electron transport and proton flux under moderate heat stress
.
Photosyn. Res.
100
,
29
43
109
Havaux
,
M.
(
1996
)
Short-term responses of photosystem I to heat stress—Induction of a PS II-independent electron transport through PS I fed by stromal components
.
Photosyn. Res.
47
,
85
97
110
Sharkey
,
T.D.
and
Weise
,
S.E.
(
2016
)
The glucose 6-phosphate shunt around the Calvin-Benson cycle
.
J. Exp. Bot.
67
,
4067
4077
111
Fisher
,
N.
,
Bricker
,
T.M.
and
Kramer
,
D.M.
(
2019
)
Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts
.
Biophys. Biochim. Acta
1860
,
148081
112
Mano
,
J.I.
,
Endo
,
T.
and
Miyake
,
C.
(
2016
)
How do photosynthetic organisms manage light stress? A tribute to the late Professor Kozi Asada
.
Plant Cell Physiol.
57
,
1351
1353
113
Asada
,
K.
(
1999
)
The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons
.
Annu. Rev. Plant Physiol. Plant Mol. Biol.
50
,
601
639
114
Habenicht
,
A.
(
1997
)
The non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase: biochemistry, structure, occurrence and evolution
.
Biol. Chem.
378
,
1413
1419
PMID:
[PubMed]
115
Scheibe
,
R.
(
2019
)
Maintaining homeostasis by controlled alternatives for energy distribution in plant cells under changing conditions of supply and demand
.
Photosyn. Res.
139
,
81
91
116
Weise
,
S.E.
,
Liu
,
T.
,
Childs
,
K.L.
,
Preiser
,
A.L.
,
Katulski
,
H.M.
,
Perrin-Porzondek
,
C.
et al (
2019
)
Transcriptional regulation of the glucose-6-phosphate/phosphate translocator 2 is related to carbon exchange across the chloroplast envelope
.
Front. Plant Sci.
10
,
827
117
Sinclair
,
T.R.
,
Rufty
,
T.W.
and
Lewis
,
R.S.
(
2019
)
Increasing photosynthesis: unlikely solution for world food problem
.
Trends Plant Sci.
24
,
1032
1039