Next Article in Journal
Physiological and Transcriptomic Analyses Reveal the Effects of Carbon-Ion Beam on Taraxacum kok-saghyz Rodin Adventitious Buds
Previous Article in Journal
A Combination of the Immunotherapeutic Drug Anti-Programmed Death 1 with Lenalidomide Enhances Specific T Cell Immune Responses against Acute Myeloid Leukemia Cells
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Research Progress in Improving Photosynthetic Efficiency

1
Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou 510642, China
2
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Life Sciences, South China Agricultural University, Guangzhou 510642, China
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2023, 24(11), 9286; https://doi.org/10.3390/ijms24119286
Submission received: 10 April 2023 / Revised: 23 May 2023 / Accepted: 24 May 2023 / Published: 26 May 2023
(This article belongs to the Section Molecular Plant Sciences)

Abstract

:
Photosynthesis is the largest mass- and energy-conversion process on Earth, and it is the material basis for almost all biological activities. The efficiency of converting absorbed light energy into energy substances during photosynthesis is very low compared to theoretical values. Based on the importance of photosynthesis, this article summarizes the latest progress in improving photosynthesis efficiency from various perspectives. The main way to improve photosynthetic efficiency is to optimize the light reactions, including increasing light absorption and conversion, accelerating the recovery of non-photochemical quenching, modifying enzymes in the Calvin cycle, introducing carbon concentration mechanisms into C3 plants, rebuilding the photorespiration pathway, de novo synthesis, and changing stomatal conductance. These developments indicate that there is significant room for improvement in photosynthesis, providing support for improving crop yields and mitigating changes in climate conditions.

1. Introduction

Photosynthesis refers to the process in which autotrophs convert light energy from the sun into chemical energy to convert inorganic carbon into complex organic carbon and release oxygen. Photosynthetic activity has enabled a large accumulation of organic matter and oxygen on Earth. Heterotrophic organisms use the organic matter and energy generated by photosynthesis to reproduce, grow, and evolve. The process of photosynthesis can be basically divided into two stages: light and dark reactions. The light-reactions stage includes the primary reaction, electron transport, and photophosphorylation; the dark-reactions stage is also called the carbon-assimilation reaction [1]. The process in which pigment molecules produce electrons by capturing solar energy is called photosynthetic electron transport (PET). PET includes linear electron transport (LET) and cyclic electron transport (CET). The light reactions of photosynthesis are the starting points of the whole photosynthesis process, providing adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide phosphate (NADPH) as the energy sources for the subsequent dark reactions, and part of the ATP and NADPH generated enters the photorespiratory pathway (Figure 1). Carbon assimilation is the carbon-reaction stage of photosynthesis, which is essentially a process of inorganic carbon fixation and conversion to organic carbon. There are various ways to fix carbon, with most autotrophs utilizing the Calvin cycle.
In recent decades, new progress has been achieved in the study of the key mechanisms of photosynthesis, but the actual efficiency of photosynthesis in converting absorbed light energy into energy substances is very low compared to theoretical values. During light reactions, photosynthesis in autotrophs is limited by the light-capture range and electron-transport efficiency. During dark reactions, the efficiency of a series of enzyme activities is low, with stomatal and mesophyll limitations, and the efficiency of converting absorbed light energy into energy substances is very low compared with the theoretical value. Improving photosynthetic efficiency involves improving light capture and conversion capacities in the light-reaction stage, optimizing the electron-transport chain, increasing Rubisco carboxylase activity, and reducing photorespiration [2].

2. Light Reactions

Light reactions occur at the chloroplast thylakoid membrane, and the reaction rate is related to the light intensity. Protein complexes on chloroplast thylakoid membranes can bind with a variety of photosynthetic pigment molecules, which absorb and transfer light energy and convert it to chemical energy (Figure 2). In higher plants, common pigment molecules include chlorophyll a, chlorophyll b, and carotenoids (β-carotene, lutein, violaxanthin, neoxanthin, etc.) [3]. These pigment molecules are excited by wavelengths of 400–700 nm in solar radiation [4] and enter the excited state from the ground state. The excited-state pigment molecules are electron donors and transfer high-energy electrons to nearby electron acceptors; the electrons obtained are coupled with the phosphate bond in the compound to convert electrical energy to chemical energy.
LET carries out classic “Z” transmission. First, the pigment P680 in the reaction center of photosystem II (PSII) is excited to produce a high-energy electron, which is transferred to the original electron acceptor magnesium-free chlorophyll. The electrons are further transferred to plastoquinone (PQ) and the cytochrome b6f complex (Cytb6f). The Cytb6f complex receives electrons and transfers H+ from the chloroplast stroma to the thylakoid lumen. Then, the electrons are transferred to plastocyanin (PC), which transfers the electrons to the reaction center pigment P700 of photosystem I (PSI). Finally, the electrons are transferred to ferredoxin (Fd), and NADP+ is converted to NADPH under the action of ferredoxin-NADP reductase (FNR) (Figure 2) [2]. In the process of LET, the H+ entering the thylakoid lumen from the chloroplast stroma and the H+ generated by photolysis of water establish the transmembrane proton potential. The chemical permeation hypothesis suggests that the chemical electromotive force of hydrogen ions inside and outside the membrane drives ATP synthesis under the action of ATP synthase [5]. CET refers to electron transfer from Fd back to PQ in plants lacking NADP+, which occurs around PSI. During this process, only ATP is synthesized, whereas NADPH is not [6] (Figure 2). Plants can change the proportion of ATP/NADPH in vivo to meet different metabolic needs through regulation between LET and CET. Research shows that after expression of CET-related genes is downregulated in plants, the photoprotection and electron transmission capacity are also significantly reduced [7]. Existing research has identified two CET pathways: the NDH (NADPH dehydrogenase)-dependent pathway [8] and the PGR5 pathway [7]. The electrons in the NDH-dependent pathway return from NDH to Fd and are then transferred to PQ and, finally, return to PSI through the Cytb6f complex and PC. After knocking out NDH in tobacco, PQ cannot be reduced, resulting in a decrease in chlorophyll fluorescence [8]. The PGR5 pathway was found in Arabidopsis mutant pgr5 and PGR5-like mutants [9,10]. The absence of the PGR5 complex in this mutant inhibits CET.

3. Increased Light-Capture Capability and Optimized Light Absorption and Conversion

Expanding the spectral range of plant photosynthesis and shortening the photosynthetic antenna complex are also important means to improve photosynthesis [11]. The effective spectral range of the light-harvesting pigment molecules in green plants is 400–700 nm, but the photosynthetic pigment molecules used by certain algae and other photosynthetic bacteria can capture and utilize near-infrared radiation with longer wavelengths (740–750 nm) [12]. Optimizing the antenna size of photosynthetic systems is one of the important directions to improve photosynthetic efficiency. Engineering and modification of pigment molecules in the light-harvesting system can increase solar-energy absorption to improve the photosynthetic rate, and with carbon assimilation efficiency also increase it with rising light-harvesting efficiency. The ATP and NADPH produced by electron transport in the photoreaction provide energy substances for the subsequent dark reactions. Under sufficient lighting conditions, the light energy that chlorophyll molecules can capture is much higher than the actual light energy utilized, and the excess absorbed light energy needs to be dissipated in other forms to avoid damage to the photosystems [13]. In leaves, this causes upper-surface cells to dissipate most of the light energy; however, the cells on the underside of the leaf lack sufficient absorption of light energy, resulting in low overall efficiency of light-energy absorption. For the whole plant, the upper leaves absorb most of the light energy [14]. Under current atmospheric conditions, shortening the antenna of light-harvesting pigment molecules can solve the problem of surface light saturation and lower-layer light deficiency. Theoretically, truncation of the chlorophyll antenna complexes of the photosystems might lead to a large increase in solar conversion efficiency [15]. Reducing chlorophyll content may also promote a more uniform distribution of light energy to increase the photosynthetic rate [16]. H. Kirst et al. shortened the antenna of photopigment molecules in cyanobacteria, improving the photosynthetic rate [17], and similar results were obtained in Arabidopsis [18]. These results suggest that shortening the antenna of photopigment molecules while maintaining the ability to adapt to fluctuating light is a potential strategy for improving photosynthesis. Cao encodes chlorophyll, which can affect the size of the antenna molecules of the photosystems [19], and the photosynthetic rate of Cao mutants obtained using RNAi technology increased more than two-fold compared with that of the wild type under strong light [20]. A shortened chlorophyll antenna also reduces non-photochemical quenching [21]. Inhibiting the YGL1 gene involved in chlorophyll synthesis and inhibiting chlorophyll synthesis can reduce antenna size and optimize light distribution [22].

4. Accelerating Recovery of NPQ (Non-Photochemical Quenching)

Any excess light during photosynthesis can lead to photooxidative damage and reduce carbon assimilation. The process of excessive excitation energy in the form of thermal energy in the PSII antenna complex is called chlorophyll fluorescence non-photochemical quenching (NPQ). Reactive oxygen species disrupt photosynthetic devices [23], and NPQ protects PSII from photoinhibition by preventing reactive oxygen species formation [24]. Heat dissipation of excess energy is activated by the electron flow of CET through acidification of the cystoid cavity, which is the main component of NPQ [25]. The change in NPQ lags behind the fluctuation of absorbed light, which is more pronounced when exposed to excessive light energy for a long time, or repeatedly [26]. This lag causes the PSII antenna to slow from a quenching to nonquenching state when the plant is exposed to high to low light intensity, and the CO2 fixation rate is briefly suppressed by NPQ. Therefore, accelerating recovery of NPQ can significantly improve canopy photosynthesis, and controlling the photoprotection pathway may be a means to improve crop stress resistance and photosynthetic productivity [11]. LHCSR1 and LHCSR2 are the main proteins that induce NPQ. When either is mutated or both are knocked down simultaneously, Chlamydomonas reinhardtii photosynthetic efficiency under intense light increased significantly [27,28]. Overexpression of NPQ-related genes in tobacco, redesigning NPQ, successfully enhances photosynthesis during natural photoconversion, increasing plant biomass by 14–20% [29]. Results similar to those in Arabidopsis were also achieved in soybean. Faster relaxation of NPQ was obtained though redesign via overexpression of related genes in soybean, and most of the transgenic lines obtained showed an obvious increase in the rate of CO2 assimilation and linear electron transport under fluctuating light conditions [30]. Introduction of a soybean-specific xanthophyll cycle in Arabidopsis accelerated NPQ recovery, resulting in an increase in PSII efficiency and a concomitant increase in the photosynthetic rate [31]. These results indicate that modulating NPQ is a feasible strategy to adjust the photosynthetic rate.

5. Improving the Cytb6f Complex

In the CET pathway, H+ is transferred to the cystoid cavity through the Cytb6f complex. The protective effect of CET on PSI depends on ΔpH [32], which regulates electron transport by acidification of the thylakoid lumen [33,34]. Acidification of the thylakoid lumen reduces the electron transport of the Cytb6f complex, resulting in a decrease in the rate from PSII to PSI [32], thus realizing the regulation of the donor side of PSI. Overexpression of the Rieske FeS protein in Arabidopsis increased the core protein level of the Cytb6f complex, resulting in an increase in the electron-transport rate and biomass yield [35]. Overexpression of the Rieske FeS subunit in Setaria viridis and obtaining plants with high expression of Cytb6f in mesophyll and bundle sheath cells increased the conversion efficiency of the light system and the thylakoid proton kinetic energy, improving the CO2 assimilation efficiency under saturated CO2 and strong light [36].

6. Dark Reactions

Carbon assimilation is the carbon-reaction stage of photosynthesis, which is essentially a process of inorganic carbon fixation and conversion to organic carbon. There are various ways to achieve carbon fixation, and most autotrophs use the Calvin cycle. Other pathways include the ribose–monophosphate pathway [37] and the 3-hydroxy-propionate pathway [38]. The Calvin cycle, also known as the C3 pathway, occurs in the chloroplast stroma. The process can be divided into CO2 fixation, reduction of carboxylation products, and regeneration of ribulose 1,5-bisphosphonate (RuBP). First, CO2 combines with RuBP under catalysis of ribulose 1,5-diphosphate carboxylase/oxygenase (Rubisco) carboxylase to form a highly unstable six-carbon compound, which randomly splits to form two molecules of 3-phosphoglycerate (PGA). Then, 3PGA receives a phosphoric acid molecule from ATP in the reaction under catalysis of phosphoglycerate kinase (PGK) to generate 1,3-diphosphoglyceride (BPGK); glyceraldehyde 3-phosphate dehydrogenase (GADPH) generates glyceraldehyde 3-phosphate (G3P) from 1,3-diphosphoglyceride and NADPH. C3 plants generate two molecules of G3P for every one molecule of CO2 fixed. However, only for every six molecules of G3P generated can one molecule of G3P enter subsequent carbon fixation, and the remaining five molecules of G3P are used for RuBP regeneration. G3P is isomerized to dihydroxyacetone phosphate (DHAP) by triose phosphate isomerase; DHAP generates fructose 1,6-diphosphate (FBP) under aldolase condensation; FBP loses one Pi molecule under catalysis of fructose diphosphatase to generate fructose 6-P (F6P); F6P is allosterically transformed to glucose 6-phosphate (G6P) under catalysis of glucose isomerase; G6P is used to form starch through a series of transformations. The Calvin cycle generates a molecule of glucose via fixation of six molecules of CO2, converting the chemical energy of ATP and NADPH generated in the light reactions to stable organic matter and using the energy supply of subsequent physiological and biochemical processes (Figure 1).

7. Modification of Rubisco

Rubisco is the most critical rate-limiting enzyme for carbon fixation in photosynthesis, playing a decisive role in the carbon-reaction rate. Rubisco is a bifunctional enzyme that not only catalyzes carbon fixation in carboxylation reactions but also produces toxic substances through oxidation reactions that need to be metabolized through photorespiration (Figure 1) [39]. In plants, Rubisco comprises the highest soluble protein content, accounting for three-quarters of all soluble proteins in C3 plants. However, its catalytic efficiency is very low, and its substrate specificity is also poor [40], which is why plants need a high Rubisco content to ensure high-speed photosynthesis. Theoretically, improving the very low catalytic activity of Rubisco can greatly improve the photosynthetic efficiency of crops [41]; hence, improving Rubisco in crops to achieve better performance is a focus of researchers. Indeed, heterologous expression of Rubisco is an important means to improve photosynthesis. Expressing the sorghum Rubisco small subunit in rice resulted in stronger catalytic activity [42]. When the Rubisco subunit of sorghum was completely replaced by the Rubisco subunit of rice, the transgenic plants obtained exhibited the characteristics of C4 plants, and the mechanical parameters related to Rubisco enzyme activity significantly increased [43]. Rubisco from Synechococcus elongatus PCC7942 introduced into tobacco can completely assemble, possesses functional activity and photosynthetic ability, and supports autotrophic growth [44]. Overexpression of Rubisco in rice led to higher photosynthetic capacity under sufficient nitrogen conditions [45]. Scientists have determined the effect of mutations on Rubisco assembly and activity through point mutation of the Rubisco large subunit in tobacco, providing more possibilities for altering Rubisco function to improve photosynthesis [46].

8. Optimization of Enzymes in the Calvin Cycle

The essence of the Calvin cycle is a series of enzyme catalysis. Therefore, in addition to improving the activity of Rubisco carboxylase, other enzymes in the Calvin cycle are important for improving photosynthetic efficiency. Carbamylation of Rubisco activase (RCA), that is, addition of carbon dioxide at the active site of lysine, is a prerequisite for activation of Rubisco [47], but premature binding of RuBP or other sugar phosphates may hinder its activity [48,49]. As the thermal instability of RCA can inhibit carbon fixation under thermal stress conditions [50], modification of RCA is also an important goal for enhancing photosynthesis. For example, increasing the thermal stability of Arabidopsis RCA can increase photosynthesis, growth rate, and biomass under moderate heat stress [51]. The more heat-resistant tobacco RCA not only has a higher photosynthetic rate under high-temperature conditions but also recovers better under normal-temperature conditions, with increased biomass and seed yield [52]. Similarly, overexpression of maize RCA in rice results in a higher activation state of Rubisco under weak light and a faster photosynthetic response when light intensity increases [53]. Transgenic plants overexpressing Rubisco and RCA in rice also have higher CO2 assimilation rates [54].
Sedoheptulose-1,7-bisphosphatase (SBPase) is an important enzyme in the Calvin cycle. It is predicted that as the concentration of carbon dioxide in the atmosphere increases, an increase in SBPase content will be beneficial for plants [55], and recent research has shown the accuracy of the prediction. For example, upregulation of the content of this enzyme in tobacco significantly improves tobacco photosynthesis and yield, and this increase in photosynthesis is more pronounced under high concentrations of carbon dioxide [56]. The photosynthetic efficiency and biomass of wheat also increases significantly when SBPase is overexpressed [57].

9. Introduction of Carbon Concentration Mechanisms into C3 Plants

According to the process of CO2 fixation with Rubisco, photosynthesis is mainly divided into three metabolic pathways: C3, C4, and CAM. Among them, the carbon concentration mechanisms (CCMs) evolving from C4 and CAM metabolism are conducive to increasing Rubisco carboxylase activity while limiting its photorespiration rate [58]. C4 plants are more efficient in utilizing light, nitrogen, and water than C3 plants [1]. CAM can increase the CO2 concentration near that of Rubisco while also reducing water evaporation and increasing water-use efficiency. Therefore, introducing C4 or CAM photosynthetic metabolic pathways into C3 plants is one of the methods to enhance photosynthesis. Mesophyll cells and vascular bundle sheath cells are two types of cells that carry out photosynthesis in C4 plants. Multiple layers of mesophyll cells surround concentrically arranged vascular bundle sheath cells to form a floral structure (Kranz anatomy). During carbon metabolism of C4 plant photosynthesis, the carboxylic acid transformation of phosphoenolpyruvate (PEP) in mesophyll cells and vascular bundle cells and continuous regeneration through transportation generates inorganic carbon with a 10-times higher concentration than that of Rubisco [59], forming CCMs; thus, the plant has higher photosynthetic efficiency. Overexpression of maize-related genes in rice leads to an increase in accumulation of photosynthetic enzymes, which means that C3 plants can be transformed to C4 plants [60]. Overexpression of the maize transcription factor GLK in rice improves photosynthetic efficiency [61]. Scientists have also confirmed that constructing C3-C4 intermediate metabolism or introducing a carboxyl matrix can improve productivity [62]. Lin et al. used tobacco as a model system to transfer two molecular chaperones from cyanobacterium Synechococcus elongatus PCC7942 (Se7942) into C3 plant chloroplasts. Tobacco can grow under high concentrations of CO2, which is an important step in introducing CCMs into vascular plant chloroplasts [63]. Long et al. successfully replaced the large and small subunit genes of Rubisco from Cyanobium with the endogenous large subunit genes of Rubisco in the chloroplast of tobacco, achieving autotrophic growth under conditions of high carbon dioxide [64] and providing a possibility for CCM engineering of C3 crop chloroplasts and improving photosynthesis. Transfer of the Rubisco large subunit of β-cyanobacterium into the Rubisco complex with the carboxyl chaperone CcmM35 in tobacco chloroplasts further demonstrates the possibility of assembling these complex CCMs in plants [65]. Rubisco derived from Halothiobacillus neapolitanus was expressed in tobacco chloroplasts, leading to the same growth rate as wild-type plants at a concentration of 1% CO2, indicating that CCMs can be applied to higher-plant Rubisco, which is an important step toward improving crop photosynthesis [66].

10. Reconstructing the Photorespiratory Pathway

Photorespiration refers to the process in which RuBP binds O2 under catalysis of Rubisco to generate 2-phosphoglycerate (2-PG) and then generate PGA (Figure 1). As photorespiration causes a large amount of carbon loss (Figure 1), reforming the photorespiratory pathway is also an important method to improve photosynthesis [40,67]. Kebeish et al. [68] were the first to introduce three enzymes involved in glycolic acid metabolism in Escherichia coli into the chloroplasts of Arabidopsis, successfully shunting glycolic acid in the chloroplasts and releasing CO2, but this approach can only improve biomass under specific conditions. A photorespiratory pathway that does not release CO2 and enhances carbon fixation was established in vitro by combining natural and artificially designed glycolate reductase [69], but this design is limited to in vitro simulation and has not been verified in planta. In tobacco, RNAi has been used to downregulate expression of glycolate transporters in chloroplasts, thereby limiting metabolites through its own pathway, reducing transport expression of glycolate and glyceric acid, and increasing the biomass of plants under field conditions by 40% [70]. Shen et al. (2019) designed a new photorespiratory pathway in rice by introducing glycolate oxidase, oxalate oxidase, and catalase into chloroplasts to enable glycolate to directly metabolize and release CO2 in the chloroplasts, that is, the photorespiratory GOC pathway. This approach significantly improved the photosynthetic efficiency and biomass of the rice plants. These results provide reliable evidence that reconstructing the photorespiratory pathway can improve the photosynthetic efficiency of rice [71].

11. Redomestication/De Novo Domestication

Genetic diversity has decreased over thousands of years of plant evolution. De novo domestication refers to the cultivation of new species from wild species [72]. Obtaining specific genes from wild plants and transferring them to cultivated plants to restore lost traits, resulting in new varieties, is called redomestication [73,74,75]. After determining the main genes involved in the regulation of photosynthesis, plants with high photosynthetic efficiency can be designed rapidly by means of de novo acclimation and genome-editing technology [76]. Transcription factors are an important target in redomestication, such as overexpression of the maize MADS-box transcription factor gene zmm28, which ultimately leads to an increase in growth, photosynthetic capacity, and nitrogen utilization [77]. With advances in genetic engineering, genome editing and synthetic biology are increasingly being widely used in various plants [78]. Scientists have determined the molecular genetic mechanism and, ultimately, a target gene by analyzing postrepresentative types of wild type and domesticated plant hybrids. For example, 14 genes directly related to the photosynthetic rate were identified by crossing 76 offspring of wild-type tomato and cultivated tomato cv M82 [79], and identification of these genes may serve as a direct goal for improving photosynthesis.

12. Changes in Stomatal and Mesophyll Conductance

In C3 plants, stomatal conductance (gs) and mesophyll conductance (gm) are important influencing factors for photosynthesis [80]. Plants absorb CO2 for photosynthesis, and gs and gm are the factors determining CO2 diffusion efficiency [81]. Gs and gm control the photosynthetic rate by affecting the CO2 concentration at carboxylation sites [82,83]. Especially under stress conditions, stomatal limitations have a higher impact on photosynthesis than biochemical limitations, such as Rubisco limitations [84]. Increasing stomatal conductance is an important means to improve photosynthetic efficiency [85]. For example, stomata are the main limiting factor for photosynthesis during the adaptation process from darkness to bright light in tobacco and Arabidopsis [86]. Stomata control absorption and transpiration of carbon dioxide at the same time, and scientists can achieve a balance between the two by changing the size and shape of the stoma and the density and distribution of mesophyll cells, thus improving photosynthesis. In fact, changing the size, shape, density, and distribution of stomata are some of the important means to improve photosynthesis [83,85]. The gene ERECTA, which regulates transpiration efficiency, can change the density, distribution, and intercellular contact to increase the rate of CO2 absorption [87]. NAL1 in rice thickens leaves by increasing the number of mesophyll cells, resulting in a significant increase in photosynthesis [88]. Increasing the density of mesophyll cells in Arabidopsis also significantly improves the photosynthetic efficiency of leaves [89]. Changing the thickness of the cell wall to affect stomatal conductance and mesophyll conductance will also be important research directions to improve photosynthetic efficiency in the future [80]. By knocking out or overexpressing genes related to regulation of stomatal development in Arabidopsis, increasing stomatal density significantly increases stomatal conductance and leaf photosynthetic rate [90]. Moreover, the open and closed states of stomata are important factors in improving photosynthetic efficiency. In mutants obtained by knocking out SLAC1, photosynthetic efficiency and stomata opening in rice were significantly higher than that of wild-type [91].

13. Conclusions

Photosynthesis is one of the most important physiological and biochemical processes on Earth, but because of the limitations of the photosynthetic autotroph system, the overall efficiency of the process is not high. Based on these restrictive factors of photosynthetic efficiency, scientists are attempting to combine genomics, transcriptomics, proteomics, metabolomics, and other methods with genome editing to improve the photosynthetic efficiency of autotrophic plants (Figure 3). The challenges involved are enormous and numerous, but the progress achieved by scientists is encouraging. In-depth study of the molecular mechanism of photosynthesis will help in understanding photosynthesis more deeply and improving the photosynthetic efficiency of plants, especially the photosynthetic efficiency of food crops, which will bring infinite possibilities for improving the yield of food crops. Photosynthetic regulation is a complex process that must be comprehensively considered to reduce negative impacts on plants, organisms, and humans.

Author Contributions

Research design, C.Z. and S.Z.; material sampling and data analysis, R.L., Y.H. and J.C.; manuscript—writing and revision, C.Z., S.Z. and R.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by grants from the open competition program of the top 10 critical priorities of Agricultural Science and Technology Innovation for the 14th Five-Year Plan of Guangdong Province (grant no. 2022SDZG05), the major program of Guangdong Basic and Applied Research (grant no. 2019B030302006), the National Natural Science Foundation of China (grant no. 32000457, 31921004), the Laboratory of Lingnan Modern Agriculture Project (grant no. NT2021002) and the Double First-class Discipline Promotion Project (grant no. 2021B10564001).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare that they have no competing interest.

Abbreviations

ATPadenosine triphosphate
BPGAglycerate 1,3-bisphosphate
CBBCalvin–Benson–Bassham
CCMscarbon concentration mechanisms
CETcyclic electron transport
Cytb6fcytochrome b6f
DHAPdihydroxyacetone phosphate
FBPasefructose 1,6-bisphosphatase
Fd,ferredoxin
F6-Pfructose 6-phosphate
GAPDHglyceraldehyde 3-phosphate dehydrogenase
gmand mesophyll conductance
GPIglucose phosphate isomerase
gsstomatal conductance
G3Pglyceraldehyde 3-phosphate
LETlinear electron transport
NADPHnicotinamide adenine dinucleotide phosphate
NPQNon-Photochemical Quenching
PCplastocyanin
PETphotosynthetic electron transport
PEPphosphoenolpyruvate
PGKphosphoglycerate kinase
PGAphosphoglycerate
PQplastoquinone
PQHsemi-plastoquinone
PSIphotosystem I
PSI-LHCIphotosystem I light-harvesting complex I
PSIIphotosystem II
PSII-LHCIIphotosystem II light-harvesting complex II
RuBPribulose 1,5-bisphosphonate
Rubiscoribulose 1,5-bisphosphate carboxylase/oxygenase
Ru5Pribulose 5-phosphate
SBPaseSedoheptulose-1,7-bisphosphatase
TPItriose phosphate isomerase
2PG2-phosphoglycerate
3-PGA3-phosphoglycerate

References

  1. Schluter, U.; Weber, A.P. The road to C4 photosynthesis: Evolution of a complex trait via intermediary states. Plant Cell Physiol. 2016, 57, 881–889. [Google Scholar] [CrossRef] [PubMed]
  2. Simkin, A.J.; Lopez-Calcagno, P.E.; Raines, C.A. Feeding the world: Improving photosynthetic efficiency for sustainable crop production. J. Exp. Bot. 2019, 70, 1119–1140. [Google Scholar] [CrossRef] [PubMed]
  3. Kusaba, M.; Maoka, T.; Morita, R.; Takaichi, S. A novel carotenoid derivative, lutein 3-acetate, accumulates in senescent leaves of rice. Plant Cell Physiol. 2009, 50, 1573–1577. [Google Scholar] [CrossRef]
  4. Baker, N.R.; Harbinson, J.; Kramer, D.M. Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ. 2007, 30, 1107–1125. [Google Scholar] [CrossRef]
  5. Mitchell, P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 1961, 191, 144–148. [Google Scholar] [CrossRef] [PubMed]
  6. Arnon, D.I.; Tsujimoto, H.Y.; McSwain, B.D. Photosynthetic phosphorylation and electron transport. Nature 1965, 207, 1367–1372. [Google Scholar] [CrossRef] [PubMed]
  7. Johnson, M.P. Metabolic regulation of photosynthetic membrane structure tunes electron transfer function. Biochem. J. 2018, 475, 1225–1233. [Google Scholar] [CrossRef]
  8. Burrows, P.A.; Sazanov, L.A.; Svab, Z.; Maliga, P.; Nixon, P.J. Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 1998, 17, 868–876. [Google Scholar] [CrossRef]
  9. Munekage, Y.; Hojo, M.; Meurer, J.; Endo, T.; Tasaka, M.; Shikanai, T. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 2002, 110, 361–371. [Google Scholar] [CrossRef]
  10. DalCorso, G.; Pesaresi, P.; Masiero, S.; Aseeva, E.; Schunemann, D.; Finazzi, G.; Joliot, P.; Barbato, R.; Leister, D. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 2008, 132, 273–285. [Google Scholar] [CrossRef]
  11. Slattery, R.A.; Ort, D.R. Perspectives on improving light distribution and light use efficiency in crop canopies. Plant Physiol. 2021, 185, 34–48. [Google Scholar] [CrossRef] [PubMed]
  12. Chen, M.; Schliep, M.; Willows, R.D.; Cai, Z.L.; Neilan, B.A.; Scheer, H. A red-shifted chlorophyll. Science 2010, 329, 1318–1319. [Google Scholar] [CrossRef] [PubMed]
  13. Melis, A. Solar energy conversion efficiencies in photosynthesis: Minimizing the chlorophyll antennae to maximize efficiency. Biotechnol. Adv. 2009, 177, 272–280. [Google Scholar] [CrossRef]
  14. Ort, D.R.; Merchant, S.S.; Alric, J.; Barkan, A.; Blankenship, R.E.; Bock, R.; Croce, R.; Hanson, M.R.; Hibberd, J.M.; Long, S.P.; et al. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl. Acad. Sci. USA 2015, 112, 8529–8536. [Google Scholar] [CrossRef]
  15. Kirst, H.; Gabilly, S.T.; Niyogi, K.K.; Lemaux, P.G.; Melis, A. Photosynthetic antenna engineering to improve crop yields. Planta 2017, 245, 1009–1020. [Google Scholar] [CrossRef]
  16. Ort, D.R.; Melis, A. Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol. 2011, 155, 79–85. [Google Scholar] [CrossRef]
  17. Kirst, H.; Formighieri, C.; Melis, A. Maximizing photosynthetic efficiency and culture productivity in cyanobacteria upon minimizing the phycobilisome light-harvesting antenna size. Biochim. Biophys. Acta 2014, 1837, 1653–1664. [Google Scholar] [CrossRef]
  18. Bielczynski, L.W.; Schansker, G.; Croce, R. Consequences of the reduction of the photosystem II antenna size on the light acclimation capacity of Arabidopsis thaliana. Plant Cell Environ. 2020, 43, 866–879. [Google Scholar] [CrossRef]
  19. Bujaldon, S.; Kodama, N.; Rappaport, F.; Subramanyam, R.; Catherine, D.V.; Takahashi, Y.; Wollman, F.A. Functional accumulation of antenna proteins in chlorophyll b-Less mutants of Chlamydomonas reinhardtii. Mol. Plant 2017, 10, 115–130. [Google Scholar] [CrossRef]
  20. Negi, S.; Perrine, Z.; Friedland, N.; Kumar, A.; Tokutsu, R.; Minagawa, J.; Berg, H.; Barry, A.N.; Govindjee, G.; Sayre, R. Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae (dagger). Plant J. 2020, 103, 584–603. [Google Scholar] [CrossRef]
  21. Kirst, H.; Melis, A. The chloroplast signal recognition particle (CpSRP) pathway as a tool to minimize chlorophyll antenna size and maximize photosynthetic productivity. Biotechnol. Adv. 2014, 32, 66–72. [Google Scholar] [CrossRef] [PubMed]
  22. Mao, L.X.; Song, Q.S.; Li, M.; Liu, X.Y.; Shi, Z.; Chen, F.M.; Chen, G.Y.; Zheng, H.Q.; Zhu, X.G. Decreasing photosystem antenna size by inhibiting chlorophyll synthesis: A double-edged sword for photosynthetic efficiency. Crop Environ. 2023, 2, 46–58. [Google Scholar] [CrossRef]
  23. Ghosh, D.; Mohapatra, S.; Dogra, V. Improving photosynthetic efficiency by modulating non-photochemical quenching. Trends Plant Sci. 2023, 28, 264–266. [Google Scholar] [CrossRef] [PubMed]
  24. Horton, P.; Johnson, M.P.; Perez-Bueno, M.L.; Kiss, A.Z.; Ruban, A.V. Photosynthetic acclimation: Does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J. 2008, 275, 1069–1079. [Google Scholar] [CrossRef] [PubMed]
  25. Takahashi, S.; Badger, M.R. Photoprotection in plants: A new light on photosystem II damage. Trends Plant Sci. 2011, 16, 53–60. [Google Scholar] [CrossRef]
  26. Muller, P.; Li, X.P.; Niyogi, K.K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 2001, 125, 1558–1566. [Google Scholar] [CrossRef]
  27. Cantrell, M.; Peers, G.A. Mutant of Chlamydomonas without LHCSR maintains high rates of photosynthesis, but has reduced cell division rates in sinusoidal light conditions. PLoS ONE 2017, 12, e179395. [Google Scholar] [CrossRef]
  28. Barera, S.; Dall’Osto, L.; Bassi, R. Effect of lhcsr gene dosage on oxidative stress and light use efficiency by Chlamydomonas reinhardtii cultures. J. Biotechnol. 2021, 328, 12–22. [Google Scholar] [CrossRef]
  29. Kromdijk, J.; Glowacka, K.; Leonelli, L.; Gabilly, S.T.; Iwai, M.; Niyogi, K.K.; Long, S.P. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 2016, 354, 857–861. [Google Scholar] [CrossRef]
  30. De, S.A.P.; Burgess, S.J.; Doran, L.; Hansen, J.; Manukyan, L.; Maryn, N.; Gotarkar, D.; Leonelli, L.; Niyogi, K.K.; Long, S.P. Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection. Science 2022, 377, 851–854. [Google Scholar]
  31. Leonelli, L.; Brooks, M.D.; Niyogi, K.K. Engineering the lutein epoxide cycle into Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2017, 114, E7002–E7008. [Google Scholar] [CrossRef] [PubMed]
  32. Yamamoto, H.; Shikanai, T. PGR5-dependent cyclic electron flow protects photosystem I under fluctuating light at donor and acceptor sides. Plant Physiol. 2019, 179, 588–600. [Google Scholar] [CrossRef]
  33. Yamori, W.; Shikanai, T. Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu. Rev. Plant Biol. 2016, 67, 81–106. [Google Scholar] [CrossRef]
  34. Shikanai, T. Regulatory network of proton motive force: Contribution of cyclic electron transport around photosystem I. Photosynth. Res. 2016, 129, 253–260. [Google Scholar] [CrossRef] [PubMed]
  35. Simkin, A.J.; McAusland, L.; Lawson, T.; Raines, C.A. Overexpression of the Rieske FeS protein increases electron transport rates and biomass yield. Plant Physiol. 2017, 175, 134–145. [Google Scholar] [CrossRef] [PubMed]
  36. Ermakova, M.; Lopez-Calcagno, P.E.; Raines, C.A.; Furbank, R.T.; Susanne, V.C. Overexpression of the Rieske FeS protein of the cytochrome b6f complex increases C4 photosynthesis in Setaria viridis. Commun. Bio. 2019, 2, 314. [Google Scholar] [CrossRef]
  37. Reizer, J.; Reizer, A.; Saier, M.H. Is the ribulose monophosphate pathway widely distributed in bacteria? Microbiology (Reading) 1997, 143 Pt 8, 2519–2520. [Google Scholar] [CrossRef]
  38. Strauss, G.; Fuchs, G. Enzymes of a novel autotrophic CO2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3-hydroxypropionate cycle. Eur. J. Biochem. 1993, 215, 633–643. [Google Scholar] [CrossRef]
  39. Peterhansel, C.; Offermann, S. Re-engineering of carbon fixation in plants—challenges for plant biotechnology to improve yields in a high-CO2 world. Curr. Opin. Biotechnol. 2012, 23, 204–208. [Google Scholar] [CrossRef]
  40. Busch, F.A. Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism. Plant J. 2020, 101, 919–939. [Google Scholar] [CrossRef]
  41. Iqbal, W.A.; Miller, I.G.; Moore, R.L.; Hope, I.J.; Cowan-Turner, D.; Kapralov, M.V. Rubisco substitutions predicted to enhance crop performance through carbon uptake modelling. J. Exper. Bot. 2021, 72, 6066–6075. [Google Scholar] [CrossRef]
  42. Ishikawa, C.; Hatanaka, T.; Misoo, S.; Miyake, C.; Fukayama, H. Functional incorporation of sorghum small subunit increases the catalytic turnover rate of Rubisco in transgenic rice. Plant Physiol. 2011, 156, 1603–1611. [Google Scholar] [CrossRef]
  43. Matsumura, H.; Shiomi, K.; Yamamoto, A.; Taketani, Y.; Kobayashi, N.; Yoshizawa, T.; Tanaka, S.I.; Yoshikawa, H.; Endo, M.; Fukayama, H. Hybrid Rubisco with complete replacement of rice Rubisco small subunits by sorghum counterparts confers C4- plant-like high catalytic activity. Mol. Plant 2020, 13, 1570–1581. [Google Scholar] [CrossRef]
  44. Lin, M.T.; Occhialini, A.; Andralojc, P.J.; Devonshire, J.; Hines, K.M.; Parry, M.; Hanson, M.R. β-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts. Plant J. 2014, 79, 1–12. [Google Scholar] [CrossRef]
  45. Tanaka, M.; Keira, M.; Yoon, D.K.; Mae, T.; Ishida, H.; Makino, A.; Ishiyama, K. Photosynthetic enhancement, lifespan extension, and leaf area enlargement in flag leaves increased the yield of transgenic rice plants overproducing Rubisco under sufficient N fertilization. Rice 2022, 15, 10. [Google Scholar] [CrossRef]
  46. Lin, M.T.; Orr, D.J.; Worrall, D.; Parry, M.; Carmo-Silva, E.; Hanson, M.R. A procedure to introduce point mutations into the Rubisco large subunit gene in wild-type plants. Plant J. 2021, 106, 876–887. [Google Scholar] [CrossRef]
  47. Lorimer, G.H.; Miziorko, H.M. Carbamate formation on the epsilon-amino group of a lysyl residue as the basis for the activation of ribulosebisphosphate carboxylase by CO2 and Mg2+. Biochemistry 1980, 19, 5321–5328. [Google Scholar] [CrossRef]
  48. Portis, A.J. Rubisco activase—Rubisco’s catalytic chaperone. Photosynth. Res. 2003, 75, 11–27. [Google Scholar] [CrossRef]
  49. Parry, M.A.; Keys, A.J.; Madgwick, P.J.; Carmo-Silva, A.E.; Andralojc, P.J. Rubisco regulation: A role for inhibitors. J. Exp. Bot. 2008, 59, 1569–1580. [Google Scholar] [CrossRef]
  50. Salvucci, M.E.; Crafts-Brandner, S.J. Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiol. 2004, 134, 1460–1470. [Google Scholar] [CrossRef]
  51. Kurek, I.; Chang, T.K.; Bertain, S.M.; Madrigal, A.; Liu, L.; Lassner, M.W.; Zhu, G. Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 2007, 19, 3230–3241. [Google Scholar] [CrossRef]
  52. Kumar, A.; Li, C.; Portis, A.J. Arabidopsis thaliana expressing a thermostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures. Photosynth. Res. 2009, 100, 143–153. [Google Scholar] [CrossRef]
  53. Yamori, W.; Masumoto, C.; Fukayama, H.; Makino, A. Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. Plant J. 2012, 71, 871–880. [Google Scholar] [CrossRef]
  54. Suganami, M.; Suzuki, Y.; Tazoe, Y.; Yamori, W.; Makino, A. Co-overproducing Rubisco and Rubisco activase enhances photosynthesis in the optimal temperature range in rice. Plant Physiol. 2021, 185, 108–119. [Google Scholar] [CrossRef]
  55. Zhu, X.G.; Eric, D.S.; Long, S.P. Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: A numerical simulation using an evolutionary algorithm. Plant Physiol. 2007, 145, 513–526. [Google Scholar] [CrossRef]
  56. Rosenthal, D.M.; Locke, A.M.; Khozaei, M.; Raines, C.A.; Long, S.P.; Ort, D.R. Over-expressing the C(3) photosynthesis cycle enzyme sedoheptulose-1–7 bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO2 fumigation (FACE). BMC Plant Biol. 2011, 11, 123. [Google Scholar] [CrossRef]
  57. Driever, S.M.; Simkin, A.J.; Alotaibi, S.; Fisk, S.J.; Madgwick, P.J.; Sparks, C.A.; Jones, H.D.; Lawson, T.; Parry, M.; Raines, C.A. Increased SBPase activity improves photosynthesis and grain yield in wheat grown in greenhouse conditions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2017, 372, 20160384. [Google Scholar] [CrossRef]
  58. Mangan, N.M.; Flamholz, A.; Hood, R.D.; Milo, R.; Savage, D.F. pH determines the energetic efficiency of the cyanobacterial CO2 concentrating mechanism. Proc. Natl. Acad. Sci. USA 2016, 113, E5354–E5362. [Google Scholar] [CrossRef]
  59. Jenkins, C.L.; Furbank, R.T.; Hatch, M.D. Mechanism of C(4) photosynthesis: A model describing the inorganic carbon pool in bundle sheath cells. Plant Physiol. 1989, 91, 1372–1381. [Google Scholar] [CrossRef]
  60. Wang, P.; Khoshravesh, R.; Karki, S.; Tapia, R.; Balahadia, C.P.; Bandyopadhyay, A.; Quick, W.P.; Furbank, R.; Sage, T.L.; Langdale, J.A. Re-creation of a key step in the evolutionary switch from C(3) to C(4) leaf anatomy. Curr. Biol. 2017, 27, 3278–3287. [Google Scholar] [CrossRef]
  61. Li, X.; Wang, P.; Li, J.; Wei, S.; Yan, Y.; Yang, J.; Zhao, M.; Langdale, J.A.; Zhou, W. Maize GOLDEN2-LIKE genes enhance biomass and grain yields in rice by improving photosynthesis and reducing photoinhibition. Commun. Biol. 2020, 3, 151. [Google Scholar] [CrossRef] [PubMed]
  62. Borden, J.S.; Savage, D.F. New discoveries expand possibilities for carboxysome engineering. Curr. Biol. 2021, 61, 58–66. [Google Scholar] [CrossRef]
  63. Lin, M.T.; Occhialini, A.; Andralojc, P.J.; Parry, M.A.; Hanson, M.R. A faster Rubisco with potential to increase photosynthesis in crops. Nature 2014, 513, 547–550. [Google Scholar] [CrossRef]
  64. Long, B.M.; Hee, W.Y.; Sharwood, R.E.; Rae, B.D.; Kaines, S.; Lim, Y.L.; Nguyen, N.D.; Massey, B.; Bala, S.; Susanne, V.C.; et al. Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts. Nat. Commun. 2018, 9, 3570. [Google Scholar] [CrossRef] [PubMed]
  65. Orr, D.J.; Worrall, D.; Lin, M.T.; Carmo-Silva, E.; Hanson, M.R.; Parry, M. Hybrid cyanobacterial-tobacco Rubisco supports autotrophic growth and procarboxysomal aggregation. Plant Physiol. 2020, 182, 807–818. [Google Scholar] [CrossRef]
  66. Chen, T.; Riaz, S.; Davey, P.; Zhao, Z.; Sun, Y.; Dykes, G.F.; Zhou, F.; Hartwell, J.; Lawson, T.; Nixon, P.J.; et al. Producing fast and active Rubisco in tobacco to enhance photosynthesis. Plant Cell 2023, 35, 795–807. [Google Scholar] [CrossRef] [PubMed]
  67. Shi, X.; Bloom, A. Photorespiration: The futile cycle? Plants 2021, 10, 908. [Google Scholar] [CrossRef] [PubMed]
  68. Kebeish, R.; Niessen, M.; Thiruveedhi, K.; Bari, R.; Hirsch, H.J.; Rosenkranz, R.; St, B.N.; Schönfeld, N.B.; Kreuzaler, F.; Peterh, N.C. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat. Biotechnol. 2007, 25, 593. [Google Scholar] [CrossRef]
  69. Trudeau, D.L.; Edlich-Muth, C.; Zarzycki, J.; Scheffen, M.; Goldsmith, M.; Khersonsky, O.; Avizemer, Z.; Fleishman, S.J.; Cotton, C.; Erb, T.J.; et al. Design and in vitro realization of carbon-conserving photorespiration. Proc. Natl. Acad. Sci. USA 2018, 115, E11455–E11464. [Google Scholar] [CrossRef]
  70. South, P.F.; Cavanagh, A.P.; Liu, H.W.; Ort, D.R. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 2019, 363, 45. [Google Scholar] [CrossRef]
  71. Shen, B.R.; Wang, L.M.; Lin, X.L.; Yao, Z.; Xu, H.W.; Zhu, C.H.; Teng, H.Y.; Cui, L.L.; Liu, E.E.; Zhang, J.J.; et al. Engineering a new chloroplastic photorespiratory bypass to increase photosynthetic efficiency and productivity in rice. Mol. Plant 2019, 12, 199–214. [Google Scholar] [CrossRef] [PubMed]
  72. Zsogon, A.; Cermak, T.; Voytas, D.; Peres, L.E. Genome editing as a tool to achieve the crop ideotype and de novo domestication of wild relatives: Case study in tomato. Plant Sci. 2017, 256, 120–130. [Google Scholar] [CrossRef] [PubMed]
  73. Palmgren, M.G.; Edenbrandt, A.K.; Vedel, S.E.; Andersen, M.M.; Landes, X.; Osterberg, J.T.; Falhof, J.; Olsen, L.I.; Christensen, S.B.; Sandoe, P.; et al. Are we ready for back-to-nature crop breeding? Trends Plant Sci. 2015, 20, 155–164. [Google Scholar] [CrossRef] [PubMed]
  74. Shelef, O.; Weisberg, P.J.; Provenza, F.D. The value of native plants and local production in an era of global agriculture. Front. Plant Sci. 2017, 8, 2069. [Google Scholar] [CrossRef] [PubMed]
  75. Wolter, F.; Schindele, P.; Puchta, H. Plant breeding at the speed of light: The power of CRISPR/Cas to generate directed genetic diversity at multiple sites. BMC Plant Biol. 2019, 19, 176. [Google Scholar] [CrossRef]
  76. Zsogon, A.; Cermak, T.; Naves, E.R.; Notini, M.M.; Edel, K.H.; Weinl, S.; Freschi, L.; Voytas, D.F.; Kudla, J.; Peres, L. De novo domestication of wild tomato using genome editing. Nat. Biotechnol. 2018, 36, 1211–1216. [Google Scholar] [CrossRef]
  77. Wu, J.; Lawit, S.J.; Weers, B.; Sun, J.; Mongar, N.; Van, H.J.; Melo, R.; Meng, X.; Rupe, M.; Clapp, J.; et al. Overexpression of zmm28 increases maize grain yield in the field. Proc. Natl. Acad. Sci. USA 2019, 116, 23850–23858. [Google Scholar] [CrossRef]
  78. Barampuram, S.; Zhang, Z.J. Recent advances in plant transformation. Methods Mol. Biol. 2011, 701, 1–35. [Google Scholar]
  79. Oliveira, S.F.; Lichtenstein, G.; Alseekh, S.; Rosado-Souza, L.; Conte, M.; Suguiyama, V.F.; Lira, B.S.; Fanourakis, D.; Usadel, B.; Bhering, L.L.; et al. The genetic architecture of photosynthesis and plant growth-related traits in tomato. Plant Cell Environ. 2018, 41, 327–341. [Google Scholar]
  80. Flexas, J.; Clemente-Moreno, M.J.; Bota, J.; Brodribb, T.J.; Gago, J.; Mizokami, Y.; Nadal, M.; Perera-Castro, A.V.; Roig-Oliver, M.; Sugiura, D.; et al. Cell wall thickness and composition are involved in photosynthetic limitation. J. Exp. Bot. 2021, 72, 3971–3986. [Google Scholar] [CrossRef]
  81. Xiong, D.; Douthe, C.; Flexas, J. Differential coordination of stomatal conductance, mesophyll conductance, and leaf hydraulic conductance in response to changing light across species. Plant Cell Environ. 2018, 41, 436–450. [Google Scholar] [CrossRef]
  82. Harrison, E.L.; Arce, C.L.; Gray, J.E.; Hepworth, C. The influence of stomatal morphology and distribution on photosynthetic gas exchange. Plant J. 2020, 101, 768–779. [Google Scholar] [CrossRef]
  83. Gago, J.; Daloso, D.M.; Carriqui, M.; Nadal, M.; Morales, M.; Araujo, W.L.; Nunes-Nesi, A.; Flexas, J. Mesophyll conductance: The leaf corridors for photosynthesis. Biochem. Soc. Trans. 2020, 48, 429–439. [Google Scholar] [CrossRef]
  84. Chen, T.W.; Stutzel, H.; Kahlen, K. High light aggravates functional limitations of cucumber canopy photosynthesis under salinity. Ann. Bot. 2018, 121, 797–807. [Google Scholar] [CrossRef]
  85. Wang, Y.; Wang, Y.; Tang, Y.; Zhu, X.G. Stomata conductance as a goalkeeper for increased photosynthetic efficiency. Curr. Opin. Biol. 2022, 70, 102310. [Google Scholar] [CrossRef]
  86. Sakoda, K.; Yamori, W.; Groszmann, M.; Evans, J.R. Stomatal, mesophyll conductance, and biochemical limitations to photosynthesis during induction. Plant Physiol. 2021, 185, 146–160. [Google Scholar] [CrossRef]
  87. Masle, J.; Gilmore, S.R.; Farquhar, G.D. The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 2005, 436, 866–870. [Google Scholar] [CrossRef]
  88. Takai, T.; Adachi, S.; Taguchi-Shiobara, F.; Sanoh-Arai, Y.; Iwasawa, N.; Yoshinaga, S.; Hirose, S.; Taniguchi, Y.; Yamanouchi, U.; Wu, J.; et al. A natural variant of NAL1, selected in high-yield rice breeding programs, pleiotropically increases photosynthesis rate. Sci. Rep. 2013, 3, 2149. [Google Scholar] [CrossRef]
  89. Lehmeier, C.; Pajor, R.; Lundgren, M.R.; Mathers, A.; Sloan, J.; Bauch, M.; Mitchell, A.; Bellasio, C.; Green, A.; Bouyer, D.; et al. Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity. Plant J. 2017, 92, 981–994. [Google Scholar] [CrossRef]
  90. Tanaka, Y.; Sugano, S.S.; Shimada, T.; Hara-Nishimura, I. Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytol. 2013, 198, 757–764. [Google Scholar] [CrossRef]
  91. Yamori, W.; Kusumi, K.; Iba, K.; Erashima, I. Increased stomatal conductance induces rapid changes to photosynthetic rate in response to naturally fluctuating light conditions in rice. Plant Cell Environ. 2020, 43, 1230–1240. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Carbon metabolism cycle diagram: the Calvin–Benson–Bassham (CBB) cycle and photorespiratory pathway. Rubisco, ribulose 1,5-bisphosphate carboxylase/oxygenase; 3-PGA, 3-phosphoglycerate; PGK, phosphoglycerate kinase; BPGA, glycerate 1,3-bisphosphate; GAPDH, glyceraldehyde 3-phosphate dehydrogenase; G3P, glyceraldehyde 3-phosphate; TPI, triose phosphate isomerase; DHAP, dihydroxyacetone phosphate; FBPase, fructose 1,6-bisphosphatase; F6-P, fructose 6-phosphate; GPI, glucose phosphate isomerase; Ru5P, ribulose 5-phosphate; 2PG, 2-phosphoglycerate; PGA, phosphoglycerate.
Figure 1. Carbon metabolism cycle diagram: the Calvin–Benson–Bassham (CBB) cycle and photorespiratory pathway. Rubisco, ribulose 1,5-bisphosphate carboxylase/oxygenase; 3-PGA, 3-phosphoglycerate; PGK, phosphoglycerate kinase; BPGA, glycerate 1,3-bisphosphate; GAPDH, glyceraldehyde 3-phosphate dehydrogenase; G3P, glyceraldehyde 3-phosphate; TPI, triose phosphate isomerase; DHAP, dihydroxyacetone phosphate; FBPase, fructose 1,6-bisphosphatase; F6-P, fructose 6-phosphate; GPI, glucose phosphate isomerase; Ru5P, ribulose 5-phosphate; 2PG, 2-phosphoglycerate; PGA, phosphoglycerate.
Ijms 24 09286 g001
Figure 2. PSI-LHCI, photosystem I light-harvesting complex I; PSII-LHCII, photosystem II light-harvesting complex II; PQ, plastoquinone; PQH, semi-plastoquinone; PC, plastocyanin; Cytb6f, cytochrome b6f; Fd, ferredoxin; NAD(P)H dehydrogenase.
Figure 2. PSI-LHCI, photosystem I light-harvesting complex I; PSII-LHCII, photosystem II light-harvesting complex II; PQ, plastoquinone; PQH, semi-plastoquinone; PC, plastocyanin; Cytb6f, cytochrome b6f; Fd, ferredoxin; NAD(P)H dehydrogenase.
Ijms 24 09286 g002
Figure 3. Ways to improve photosynthetic efficiency: optimizing light reactions; optimizing enzymes in the Calvin cycle; introducing CCMs; engineering photorespiration; synthetic biology; de novo domestication; increasing stomatal conductance and mesophyll conductance.
Figure 3. Ways to improve photosynthetic efficiency: optimizing light reactions; optimizing enzymes in the Calvin cycle; introducing CCMs; engineering photorespiration; synthetic biology; de novo domestication; increasing stomatal conductance and mesophyll conductance.
Ijms 24 09286 g003
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Li, R.; He, Y.; Chen, J.; Zheng, S.; Zhuang, C. Research Progress in Improving Photosynthetic Efficiency. Int. J. Mol. Sci. 2023, 24, 9286. https://doi.org/10.3390/ijms24119286

AMA Style

Li R, He Y, Chen J, Zheng S, Zhuang C. Research Progress in Improving Photosynthetic Efficiency. International Journal of Molecular Sciences. 2023; 24(11):9286. https://doi.org/10.3390/ijms24119286

Chicago/Turabian Style

Li, Ruiqi, Ying He, Junyu Chen, Shaoyan Zheng, and Chuxiong Zhuang. 2023. "Research Progress in Improving Photosynthetic Efficiency" International Journal of Molecular Sciences 24, no. 11: 9286. https://doi.org/10.3390/ijms24119286

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop