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Review

Physiological Factors Limiting Leaf Net Photosynthetic Rate in C3 Crops like Rice and Approaches for Improving It

by
Miao Ye
,
Meng Wu
,
Yu Zhang
,
Zeyu Wang
,
Hao Zhang
and
Zujian Zhang
*
Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Jiangsu Key Laboratory of Crop Cultivation and Physiology, Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(8), 1830; https://doi.org/10.3390/agronomy12081830
Submission received: 15 June 2022 / Revised: 22 July 2022 / Accepted: 30 July 2022 / Published: 2 August 2022
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Abstract

:
Improving leaf photosynthetic capacity is one of the most promising approaches to further boost crop yield. Clarifying factors limiting leaf photosynthetic capacity, especially in C3 crops, is meaningful for designing strategies to improve it. Leaf net photosynthetic rate (A) is one of the parameters describing leaf photosynthetic capacity. In the present study, physiological factors limiting A in C3 crops such as rice were discussed and different approaches for A improvement were summarized to provide theoretical guidance for increasing leaf photosynthetic capacity. A will be limited by both CO2 availability and light intensity over periods from a few hours to several days, and by one of them over shorter intervals. Under current ambient atmospheric conditions, A of C3 crops is mainly limited by Rubisco activity and the CO2 concentration in chloroplasts. Leaf nitrogen content affects A by regulating Rubisco content and leaf anatomy; leaf morphological and anatomical traits limit A by impacting stomatal and mesophyll CO2 diffusion. Further improvements of A in C3 crops can be achieved by designing or introducing high-activity Rubisco; adjusting leaf nitrogen allocation to optimize leaf anatomy and leaf chemical composition; modifying leaf morphology and anatomy for greater CO2 diffusion; improving the activity of proteins and enzymes associated with sugar transportation and utilization; introducing C4 photosynthetic mechanisms and combining high photosynthetic traits by conventional breeding.

1. Introduction

The leaf net photosynthetic rate (A, μmol (CO2) m−2 s−1) is defined as the amount of CO2 assimilated by 1 m2 leaf per 1 s and is calculated as follows:
A = V c − 0.5 V o − R d
where Vc is the velocity of ribulose-1,5-bisphosphate (RuBP) carboxylation; Vo is the rate of oxygenation, Vo is multiplied by 0.5 because half a mole of CO2 is evolved for every mole of oxygenation event; Rd is the day respiration rate, which is referred to the mitochondrial respiration rate under light.
A will be limited by both CO2 availability and light intensity over periods from a few hours to several days, and by one of them over shorter intervals [1]. The Farquhar-von Caemmerer-Berry (FvCB) model for C3 photosynthesis assumes that carboxylation of RuBP by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is limited by one of three factors: (1) the activity of Rubisco; (2) the RuBP regeneration rate; and (3) the release of phosphate during the metabolism of triose phosphate to either starch or sucrose (rate of triose-phosphate utilization, TPU) [2,3,4,5]. Under low CO2 conditions, sufficient nicotinamide adenine dinucleotide phosphate (NADPH) and adenosine triphosphate (ATP) are produced by the light reaction, and A linearly increases with the intercellular CO2 concentration (Ci) (Figure 1). At this time point, A is mainly limited by the activity of Rubisco. As Ci increases, ATP is insufficient to regenerate adequate RuBP, thereby increasing A with Ci decreases (Figure 1). Thus, A is mainly limited by the RuBP regeneration rate. As Ci further increases, triose-phosphate in the chloroplasts is redundant and will inhibit A as a feedback mechanism [6] (Figure 1). Then, A is mainly limited by TPU.
Under current ambient atmospheric conditions (400 μmol (CO2) mol−1 (air)), the A of C3 crops is mainly limited by Rubisco carboxylation capacity, which is related to both the content and the specific activity of Rubisco [7,8]. Rubisco is a type of bifunctional enzyme that can catalyze both carboxylation and oxygenation reactions and CO2 competes with O2 as a substrate for Rubisco. The carboxylation and oxygenation rate depends on the affinity of Rubisco for CO2 and O2 as well as the ratio of CO2 and O2 concentrations in chloroplasts. The low solubility of CO2 in water at ambient temperatures means dissolved CO2 in equilibrium with atmospheric CO2 in the range of 10–20 μM, well below the Michaelis constant for carboxylation reaction (Kc) of C3 Rubisco, although the Michaelis constant for oxygenation reaction (Ko) (typically higher than 300 μM) is far higher than Kc [9,10,11]. Therefore, the affinity of Rubisco for CO2 and the CO2 concentration in chloroplasts (Cc) represent the main limiting factors for A in C3 crops under natural conditions [12,13,14,15,16].

2. Physiological Factors Limiting Leaf Net Photosynthetic Rate in C3 Crops

2.1. Effects of Rubisco on Leaf Net Photosynthetic Rate

Rubisco is the most abundant enzyme in plants, accounting for approximately 40% of soluble proteins in leaves; 22–33% of leaf nitrogen (N) is allocated to Rubisco in the typical C3 crop—rice [17,18]. Although Rubisco is redundant under high CO2, low temperature, or low light conditions [18,19,20,21,22], A significantly increases with Rubisco content under normal conditions [23]. Increasing the leaf N content can remarkably increase the Rubisco content, improve the total activity of Rubisco, and finally enhance A [16,24]. However, Suzuki et al. [25] found that greater allocation of N to Rubisco in rice decreased the allocation of N to other proteins and enzymes associated with the tricarboxylic acid cycle and consequently decreased A.
As CO2 and O2 compete to use one site on Rubisco to process carboxylation and oxygenation, the ratio of Vc and Vo is expressed as follows [9]:
V c V o = k c k o × K o K c × [ CO 2 ] [ O 2 ]
where kc and ko are the turnover rate constants for carboxylation and oxygenation reactions, respectively, and the unit is mol mol−1 (site) s−1. [CO2] and [O2] are the CO2 and O2 concentrations in chloroplasts, respectively, and the unit is μmol mol−1. The specificity of Rubisco (Sc/o) is expressed as follows [9]:
S c / o = k c k o × K o K c = k c K o k o K c
Sc/o is greatly affected by temperature, increasing with temperatures between 15–30 °C and decreasing with temperatures above 30 °C [9,26].
Sc/o differs greatly between species, for example, in Rhodospirillum rubrum it is only 12.3, in rice it is 85, but in Griffithsia monilis it reaches 167 under 25 °C [10]; hence, studies have attempted to introduce high-activity Rubisco to C3 crops to improve their photosynthetic capacity. Lin et al. [27] introduced Rubisco from cyanobacteria into tobacco plants, however, the transgenic plants did not survive under normal atmospheric CO2 concentration. Introducing high-efficiency Rubisco, for example from Griffithsia monilis to C3 crops to improve the carboxylation efficiency needs more investigation.

2.2. Effects of Leaf Nitrogen Content on Leaf Net Photosynthetic Rate

Mass-based (Nmass) or area-based (Narea) leaf N content is expressed to represent leaf N content (LNC). In addition to affecting Rubisco content, LNC can affect leaf photosynthesis by impacting other factors. Taylaran et al. [28] reported that increasing Narea can significantly improve stomatal conductance (gs) and finally enhance A in rice. Moreover, LNC can alter leaf anatomy. Polesskaya et al. [29] found that leaf and leaf cell walls became thick under N deficit conditions, and the cell wall under ammonium N was thicker than that under nitrate N. Li et al. [30] reported that the chloroplast size under high N supply (HN) was larger than that under low N supply (LN), and Rubisco content also increased with chloroplast size in C3 plant rice. Xiong et al. [31] demonstrated that the cell wall under HN was thinner than that under LN, whereas the surface area of cells exposed to intercellular airspace (IAS) per leaf area (Sm) and the surface area of chloroplasts exposed to IAS per leaf area (Sc) under HN were both higher than those under LN in rice. The thin cell wall and high Sm and Sc promoted mesophyll CO2 diffusion and improved A.
To enhance the understanding of the intrinsic relationship between A and LNC, the concept of photosynthetic nitrogen utilization efficiency (PNUE) was established. PNUE is the ratio of A to Narea. Improving PNUE can be achieved by improving A, decreasing Narea, or promoting a larger increase in A than in Narea. To avoid N loss and environmental pollution caused by excessive N application, scientists have proposed “N reducing” strategies, including site-specific N management (SSNM) for crops [32]. Reducing N application means that Narea will likely decrease, and PNUE will subsequently increase. Therefore, it is particularly important to breed cultivars exhibiting high A under low Narea. It was reported that in the field, N needs to be applied to improve crop yield when the Narea of the newest fully expanded leaf is less than 1.40 g m−2 [32]. Coincidentally, Ye et al. [33] found that Narea did not contribute to the improvement in A when Narea was greater than 1.40 g m−2, and PNUE was positively correlated with A across 121 cultivated rice lines. In Ye et al. [33], the 121 rice lines were divided into four sections according to their leaf net photosynthetic rate, and it can be found that only when A was lower than 20 μmol m−2 s−1 the average Narea was lower than those of other sections (Table 1). These findings indicated that when A is higher than 20 μmol m−2 s−1, the further improvement in A was not attributed to the increase in Narea, it is possible to select varieties showing both high PNUE and high A. How to regulate other limiting factors for A, such as CO2 diffusional conductance, by adjusting N application to further improve A requires more investigations.

2.3. Effects of Stomatal Conductance on Leaf Net Photosynthetic Rate

Diffusing from air to the carboxylation sites, CO2 first needs to overcome the boundary resistance between air and leaf to reach the leaf surface, and then enters the stomatal pores to reach the substomatal cavity (Figure 2a). CO2 diffusional resistance from the leaf surface to the substomatal cavity is referred to as stomatal resistance (rs) and the reciprocal of rs is called stomatal conductance (gs).
CO2 entering a leaf and H2O evaporating from a leaf both need to pass through the stomatal pores. gs is usually obtained by measuring the stomatal conductance to H2O (gsw), gs = gsw/1.6, as the diffusing rate of H2O in the air is 1.6 times that of CO2. gs is mainly determined by stomatal size, stomatal density, stomatal distribution, and especially by stomatal aperture [34,35]. Large stomatal pores and stomatal apertures as well as high stomatal density were suggested to be of benefit for improving gs and A in species [36,37,38,39]. As an important determinant for gs, the stomatal aperture is greatly influenced by plant hydraulic status [40,41]. A, gs, and transpiration rate (E) were found to be positively correlated with the plant hydraulic conductance [42].
As leaf hydraulic resistance accounts for greater than one-quarter of whole-plant hydraulic resistance [43,44], leaf hydraulic conductance (Kleaf), the reciprocal of leaf hydraulic resistance, determines leaf gas exchange parameters greatly [40,45,46]. In higher plants, water from the stem moves into the petiole through the xylem in different vein orders, then passes through the bundle sheath and the mesophyll tissue before evaporating into the IAS and diffusing out of the leaf from the stomatal pores [47,48]. Therefore, leaf hydraulic transport can be divided into two parts—xylem hydraulic transport and outside-xylem hydraulic transport.
As leaf hydraulic transport consists of the xylem and outside xylem hydraulic transports, Kleaf is mainly determined by leaf vein and mesophyll anatomical traits [48,49]. High leaf vein density, short distances between veins and stomata, large xylem conduit diameters, high Sm, Sc, and the fraction of intercellular airspace (fias) as well as thin cell walls were reported to be beneficial for improving Kleaf [46,48,50].
In addition to leaf hydraulic resistance, root hydraulic resistance also significantly accounts for approximately one-third to half of the whole-plant hydraulic resistance [51,52]. Thus, Kroot, the reciprocal of root hydraulic resistance, was also found to impact A. Else et al. [53] found that a reduction in Kroot can decrease the leaf water potential and cause stomatal closure in Ricinus communis plants. Some species growing in flooded conditions, for instance, rice, form numerous aerenchyma in leaves, stems, and roots to transport O2. To reduce the outward diffusion of O2 in the root aerenchyma, a layer of wood components was formed on the root surface in rice plants, which greatly decreased the Kroot [54]. In addition, the formation of aerenchyma will reduce the effective area for radial water transport, which will also decrease Kroot [55]. Moreover, aquaporins (AQPs) are also involved in regulating Kroot [56]. Thus, traits that affect Kroot mainly include the root surface area, the degree of lignification, and the expression of AQPs [57,58,59,60].

2.4. Effects of Mesophyll Conductance on Leaf Net Photosynthetic Rate

After reaching the substomatal cavity, CO2 needs to diffuse to the surroundings of the cell wall, then successively passes through the cell wall, plasmalemma, cytosol, chloroplast envelope, and stroma to get to the carboxylation sites [12] (Figure 2b). The CO2 diffusional resistance from the substomatal cavity to the carboxylation sites is referred to as mesophyll resistance (rm). rm limits photosynthesis to the same magnitude as rs under many conditions [61,62]. The reciprocal of rm is called mesophyll conductance (gm). A was found to be positively correlated with both gm and gs in numerous previous studies [63,64].
gm is greatly determined by leaf anatomical traits [12,62]. Many anatomical properties were reported to determine gm, including the fraction of intercellular airspace (fias), the surface area of cells exposed to intercellular airspace (IAS) per leaf area (Sm), the surface area of chloroplasts exposed to IAS per leaf area (Sc), and cell wall thickness (Tcw). High Sm, Sc, and fias were suggested to be of benefit for improving gm [48,63,65,66,67,68,69]. Among these anatomical traits, Tcw is particularly important for determining gm given that cell wall resistance accounts for about half of the total mesophyll resistance [62] and gm was found to be negatively correlated with Tcw in many species [65,66,67,70,71,72].
Leaf mass per area (LMA), a composite parameter describing leaf anatomy, is defined as the leaf dry weight per leaf area. Some studies reported that LMA was negatively correlated with gm [69,70,73], and it was suggested to be related to Tcw and IAS [67,74]. High LMA is usually accompanied by a thicker cell wall [67,71,74]. Ye et al. [71] found that high LMA rice genotypes showed low gm mainly due to the relatively thick cell wall but not high Sm and Sc. However, some studies also found that gm did not correlate with LMA [68,75,76,77,78], which may be due to different physiological and biochemical features.
Apart from leaf anatomy, leaf biochemical components (e.g., carbonic anhydrase (CA) and AQPs) were also found to be involved in regulating gm [79,80]. CO2 needs to dissolve in the apoplastic water of the cell wall to pass through the cell wall as HCO 3 − , and the conversion from CO2 to HCO 3 − is catalyzed by CA located external to the cell membrane [62,81,82]. AQPs are a family of membrane-bound water channel proteins that play a major role in regulating the water transport distribution in leaves [83,84]. Recently, an increasing number of studies have found that AQPs also participate in regulating CO2 diffusion across membranes [12,80,85]. Some AQP genes, such as NtAQP1 and AtPIP1;2, were found to play roles in CO2 diffusion across membranes [86,87,88].
In addition to leaf anatomy, CA, and AQPs, other factors, such as leaf chemical composition, have also been reported to affect gm. Ye et al. [71] demonstrated that increased investment of leaf mass to the cell wall leads to low gm in rice plants. A more recent study also reported that changes in cell wall composition, particularly in pectin content, determined leaf elasticity in both gs and gm [89]. The influence of cell wall composition on gm and photosynthesis has started to attract attention in recent years. For example, Flexas et al. [90] summarized the effects of cell wall structure and composition on leaf photosynthesis and proposed the idea of improving leaf photosynthesis by manipulating the cell wall, e.g., improving the mesophyll conductance and photosynthetic rate by decreasing cell wall thickness and reducing cellulose. Improving gm and A in C3 crops by altering leaf anatomy and leaf chemical composition requires further investigation.
Furthermore, based on the determinants for Kleaf and gm, we can know that Kleaf and gm are both affected by leaf anatomical traits fias, Sm, Sc, and Tcw. Thus, gm was found to be positively correlated with Kleaf [48]. However, although Xiong et al. [48] explained that the coordination between gm and Kleaf is partly attributed to the shared diffusion pathways of CO2 and H2O inside leaves, the complete mechanisms remain unclear, i.e., the location of evaporating sites. Canny et al. [91] reported that cells in the spongy mesophyll and palisade cells surrounding substomatal cavities shrank more in size compared to the majority of cells in the palisade tissue during initial dehydration, indicating that H2O mainly evaporates from the spongy mesophyll and palisade cells surrounding substomatal cavities. However, Rockwell et al. [47] reported that the H2O dominantly evaporates from the vascular bundle sheath and its surroundings to the IAS in Quercus rubra. The H2O diffusion pathway inside leaves and its coordination with gm require further investigation.

2.5. Effects of the Rate of Sugar Utilization on Leaf Net Photosynthetic Rate

Although the A of C3 crops is mainly limited by the activity of Rubisco and Cc under natural conditions, it is still affected by the rate of triose-phosphate utilization. The quantity of triose-phosphate transported from the chloroplasts to the cytoplasm is regulated by the Pi level in the cytoplasm. The triose-phosphate was transported out of the chloroplast by the Pi transporter on the envelope, at the same time, equal amounts of Pi are transported from the cytoplasm to the chloroplast. When the triose-phosphate forms the sucrose in the cytoplasm, Pi is released. If the transport of sucrose from the cytoplasm is restricted, or the utilization decreases, the transport of triose-phosphate from the chloroplast will be restricted, and finally, inhibit photosynthesis. During the triose-phosphate utilization process, sucrose phosphate synthase (SPS) plays an important role [92], while sucrose transporter and SWEET protein on plasmalemma and cell wall invertase play pivotal roles during the apoplast transport of sucrose [93,94,95].

2.6. Response of Leaf Photosynthesis to Changing Environments

Above we generally talked about the factors limiting the instantaneous CO2 assimilation rate. However, steady-state conditions are rare in nature, and growth environments, especially irradiance, are intrinsically heterogeneous in time and space within canopies. Leaves within a canopy experience a highly variable light environment in magnitude (PAR 1–2000 μmol m−2 s−1) and time (seconds to minutes or longer) over the course of a day due to changes in the incoming solar irradiance, cloud cover, wind, and self-shading of the upper leaves [96,97]. When shifting from low irradiance to high irradiance, the recovery of Rubisco activity and stomatal and mesophyll conductance are crucial for the recovery of leaf photosynthesis [97]. Generally, the full activation of Rubisco needs 10–30 min, which strongly restricts the recovery of photosynthesis. Recently, Zhang et al. [98] found that the increasing rate of light-induced stomatal conductance is related to stomatal size in the genus Oryza, as small stomata are not beneficial for the rapid activation of Rubisco. How the adaption of leaf physiological properties to changing irradiance affects leaf photosynthetic capacity needs more investigation.
Except for irradiance, other environmental factors such as temperature also change in nature, although it changes much slower and to a smaller degree. Temperature responses of photosynthesis have also attracted attention. Studies showed that the temperature response of photosynthesis is strongly determined by the temperature response of mesophyll conductance [72,99]. Regarding the underlying mechanisms of the temperature response of mesophyll conductance, classic hypotheses have been proposed. Bernacchi et al. [100] illustrated that CA and aquaporins are candidates for determining the temperature response of gm, while Xiong et al. [31] suggested that the rapid temperature response of gm is related to the regulation of diffusion through biological membranes but not the response of leaf structure. Recently, Li et al. [101] reported that leaf water potential (Ψleaf) plays important role in determining the temperature response of gm and they revealed that the decline of Ψleaf with leaf temperature is one of the reasons for the decreasing of gm with temperature. Except for these hypotheses, other models including the two components model [102] and the optimal gmem (membrane conductance to CO2) model [103] have also been established to investigate the temperature response of gm. Recently, Ye et al. [72] reported that the stronger response of gm to temperature was related to the larger activation energy of membrane in rice. Factors limiting the responding rate of photosynthesis to temperature need more investigation.

3. Approaches for Improving Leaf Net Photosynthetic Rate in C3 Crops

According to equation 1, we know that improving the carboxylation rate and decreasing the respiration rates can both increase A. However, recent studies demonstrated that depressing the photorespiration or the day respiration both affected the nitrogen metabolism in plants and reduced the quality of crop products [104,105,106]. In addition, under stressed conditions such as high light intensity, drought, or salt stress, the photorespiration can consume the redundant NADPH, reducing the peroxide production, thus protecting the photosynthetic apparatus [107,108,109]. Moreover, the glycine and serine produced during the photorespiration process also participate in plant metabolism [110] and photorespiration is necessary for plant growth and development. Modifying Rubisco to depress respiration by gene engineering is not of benefit for plant growing [111].
Whether improving the carboxylation rate or decreasing the respiration consumption, the final aim is to improve the photosynthetic capacity. Many gene engineering approaches were suggested to improve the photosynthetic capacity, for example, designing efficient Rubisco or improving the heat tolerance of the Rubisco kinase to keep the Rubisco efficient even under high temperatures [27,112,113,114,115,116]; improving the activities of the enzymes associated with the Calvin cycle, e.g., fructose-1,6-bisphosphatase (FBPase) and sedoheptulose 1,7-bisphosphatase (SBPase), to improve the carboxylation rate [117,118,119,120,121,122]; improving the electron transport rate on the thylakoid membranes [123,124,125]; introducing CO2 concentrating mechanisms or the Kranz anatomy from C4 plants to C3 crops [126,127,128,129]; modifying leaf morphology and anatomy to improve the light capturing and the CO2 diffusion [130,131,132,133]. Alternatively, based on the natural variations of photosynthetic characteristics in the plant germplasm, combining high photosynthetic traits through traditional breeding can also improve photosynthetic capacity [16].
Under natural conditions, the A of C3 crops is usually lower than that of C4 plants, as A of C3 crops is usually lower than 40 μmol m−2 s−1, while it is commonly higher than 40 μmol m−2 s−1 in C4 plants [16,134,135]. There is no doubt that the A of C3 crops will be greatly improved if the C3 crops were modified into C4 plants. The phosphoenolpyruvate carboxylase (PEPC) in C4 plants, which catalyzes the reaction between phosphoenolpyruvate (PEP) and HCO 3 − , has a higher affinity for HCO 3 − than Rubisco for CO2. Sheehy et al. [136] illustrated that the success of building C4 rice can improve the rice yield by 50%. The International Rice Research Institute (IRRI) also started ‘The C4 Rice Project’ from 2008 (https://c4rice.com/the-project-2/our-history/), aimed at building C4 rice. Taniguchi et al. [137] introduced the PEPC, pyruvate, orthophosphate dikinase (PPDK), and malate dehydrogenase (MDH) from maize to rice plants, however, the gene-modified rice plants did not show an increase in A, the A of gene-modified rice plants even showed lower A than that of wild plants, due to an increasing photorespiration rate. Lacking knowledge about the genetic control of Kranz anatomy and dimorphic chloroplast formation, and detailed information about the regulation of cellular metabolism and metabolite trafficking between cellular compartments, there are still great obstacles to building C4 rice [138]. However, although it is a big challenge, progress has still been made with C4 rice engineering, for instance, the flux of CO2 fixation by PEPC was increased within C4 transgenic rice [139,140].
Moreover, although it is difficult to switch from C3 crops to C4 plants in a short time, there are still some conservative approaches to improve the A in C3 crops, such as combining high photosynthetic traits by traditional breeding work to build plants with higher A. Adachi et al. [16] identified two rice lines with extremely high values of A among the backcrossed inbred lines derived from the indica variety Takanari, one of the most productive varieties in Japan, and the elite japonica variety Koshihikari (Koshihikari/Takanari//Takanari). Combining the advantages of small mesophyll cells and more developed lobes of mesophyll cells from Koshihikari, high Kroot, strong nitrogen accumulation capacity, and thick mesophyll from Takanari, the A of the two lines reached 38.8 μmol m−2 s−1 and 37.6 μmol m−2 s−1, respectively, significantly higher than their parents, which were 30.8 μmol m−2 s−1 and 24.4 μmol m−2 s−1. Thus, selecting varieties with high photosynthetic traits and combining them together can further improve the photosynthetic rate in C3 crops.
Therefore, according to the factors limiting the A and attempts made to improve the A in C3 crops, we can summarize approaches to improving the A in C3 crops: design or introduce high-activity Rubisco; adjust leaf nitrogen allocation to optimize leaf anatomy and leaf chemical composition; modify leaf morphology and anatomy for greater CO2 diffusion; improve the activity of proteins and enzymes associated with sugar transportation and utilization; introduce C4 photosynthetic mechanisms to C3 crops and combine high photosynthetic traits by conventional breeding (Figure 3).

4. Conclusions

Under current ambient atmospheric conditions, the leaf net photosynthetic rate of C3 crops is mainly limited by Rubisco activity and the CO2 concentration in chloroplasts. Leaf nitrogen content affects leaf net photosynthetic rate by regulating Rubisco content and leaf anatomy; leaf morphological and anatomical traits including stomatal size, stomatal density, stomatal distribution, leaf vein density, leaf vein diameter, the fraction of intercellular airspace, the surface area of cells exposed to intercellular airspace (IAS) per leaf area, and the surface area of chloroplasts exposed to IAS per leaf area and cell wall thickness limit leaf net photosynthetic rate by impacting stomatal and mesophyll CO2 diffusion. Further improvements in leaf net photosynthetic rate in C3 crops can be achieved by designing or introducing high-activity Rubisco; adjusting leaf nitrogen allocation to optimize leaf anatomy and leaf chemical composition; modifying leaf morphology and anatomy for greater CO2 diffusion; improving the activity of proteins and enzymes associated with sugar transportation and utilization; introducing C4 photosynthetic mechanisms, combining high photosynthetic traits by conventional breeding, etc.

Author Contributions

M.Y. designed the frame of the manuscript and wrote it. M.W., Y.Z. and Z.W. participated in writing the physiological factors limiting leaf net photosynthetic rate part. H.Z. and Z.Z. commented and revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the China Postdoctoral Science Foundation (2021M702769); the R&D Foundation of Jiangsu province, China (BE2022425, BK20220017) and the National Natural Science Foundation of China (31871559).

Acknowledgments

We would like to express our heartfelt appreciations to the Jiangsu Funding Program for Excellent Postdoctoral Talent.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 01830 g001 550
Figure 1. The A/Ci curve of rice leaf. A, leaf net photosynthetic rate; Ci, intercellular CO2 concentration.
Figure 1. The A/Ci curve of rice leaf. A, leaf net photosynthetic rate; Ci, intercellular CO2 concentration.
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Figure 2. The diffusing pathway of CO2 from the atmosphere to the chloroplast. (a) The light microscope image of rice leaf and (b) the transmission electron microscope image of rice leaf. Ca, atmospheric CO2 concentration; Ci, intercellular CO2 concentration; Cc, chloroplastic CO2 concentration; gs, stomatal conductance to CO2; gm, mesophyll conductance to CO2.
Figure 2. The diffusing pathway of CO2 from the atmosphere to the chloroplast. (a) The light microscope image of rice leaf and (b) the transmission electron microscope image of rice leaf. Ca, atmospheric CO2 concentration; Ci, intercellular CO2 concentration; Cc, chloroplastic CO2 concentration; gs, stomatal conductance to CO2; gm, mesophyll conductance to CO2.
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Figure 3. Physiological factors limiting leaf photosynthetic capacity in C3 crops under natural conditions and approaches for improving it.
Figure 3. Physiological factors limiting leaf photosynthetic capacity in C3 crops under natural conditions and approaches for improving it.
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Table
Table 1. The average leaf net photosynthetic rate (A) and area-based leaf nitrogen content (Narea) of 121 cultivated rice lines in different sections.
Table 1. The average leaf net photosynthetic rate (A) and area-based leaf nitrogen content (Narea) of 121 cultivated rice lines in different sections.
SectionA (μmol m−2 s−1)Narea (g m−2)Number of Rice Lines
A ≥ 3031.5 ± 0.9 a1.67 ± 0.17 a5
25 ≤ A < 3027.0 ± 1.5 b1.57 ± 0.16 a34
20 ≤ A < 2522.4 ± 1.4 c1.53 ± 0.18 a60
A < 2018.4 ± 1.2 d1.35 ± 0.22 b22
The data followed by different letters are significant at p < 0.05 level.
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Ye, M.; Wu, M.; Zhang, Y.; Wang, Z.; Zhang, H.; Zhang, Z. Physiological Factors Limiting Leaf Net Photosynthetic Rate in C3 Crops like Rice and Approaches for Improving It. Agronomy 2022, 12, 1830. https://doi.org/10.3390/agronomy12081830

AMA Style

Ye M, Wu M, Zhang Y, Wang Z, Zhang H, Zhang Z. Physiological Factors Limiting Leaf Net Photosynthetic Rate in C3 Crops like Rice and Approaches for Improving It. Agronomy. 2022; 12(8):1830. https://doi.org/10.3390/agronomy12081830

Chicago/Turabian Style

Ye, Miao, Meng Wu, Yu Zhang, Zeyu Wang, Hao Zhang, and Zujian Zhang. 2022. "Physiological Factors Limiting Leaf Net Photosynthetic Rate in C3 Crops like Rice and Approaches for Improving It" Agronomy 12, no. 8: 1830. https://doi.org/10.3390/agronomy12081830

APA Style

Ye, M., Wu, M., Zhang, Y., Wang, Z., Zhang, H., & Zhang, Z. (2022). Physiological Factors Limiting Leaf Net Photosynthetic Rate in C3 Crops like Rice and Approaches for Improving It. Agronomy, 12(8), 1830. https://doi.org/10.3390/agronomy12081830

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