Open access peer-reviewed chapter
Abstract
Phosphorus (P) is an essential mineral nutrient for plant growth and development, second only to nitrogen in abundance. It is frequently limited in soil, requiring the application of P-fertilizers to improve plant productivity. One critical function of P in plants is its role in the dark phase of photosynthesis, where it functions in energy storage and transfer, carbon fixation, regulation of the dark phase, and nucleotide and coenzyme biosynthesis. P is a foundational component of important molecules like ATP and essential coenzymes, which are crucial for efficient carbon fixation and energy conversion during the Calvin cycle. Sustainable P-management strategies and improved agricultural practices are necessary to optimize plant growth and ensure sustainable agricultural production in the face of P-limitations.
Keywords
- Calvin-Benson-Bassham (CBB) cycle
- phosphorylation
- adenosine triphosphate
- nicotinamide adenine dinucleotide phosphate
- phosphorus
- photophosphorylation
1. Introduction
Photosynthesis is the process by which plants, algae, and some bacteria convert light energy into chemical energy in the form of glucose and other organic molecules [1]. This process is essential for the survival of nearly all life on Earth, as it forms the basis of the food chain and is responsible for the production of oxygen in the atmosphere [2]. Photosynthesis consists of two main phases: the light-dependent reactions, which occur in the thylakoid membranes of the chloroplasts and generate ATP and NADPH; and the light-independent reactions, also known as the dark phase or the Calvin-Benson-Bassham (CBB) cycle, which occur in the stroma of the chloroplasts and utilize the ATP and NADPH produced in the light-dependent reactions to fix CO2 into organic molecules [3].
Phosphorus (P) is an essential element for all living organisms, as it is a key component of several biomolecules, such as nucleic acids, ATP, and phospholipids. P is beneficial to plants both in its elemental form and as a component of other molecules such as phosphates. After nitrogen (N), P is quantitatively the most significant inorganic nutrient for plant growth, and often limits primary productivity in natural systems as well as agricultural systems, unless supplied as fertilizer [4]. In plants, P plays a crucial role in various physiological processes, including energy metabolism, nucleic acid synthesis, and membrane function, as well as in the regulation of enzyme activity and signal transduction pathways [5, 6]. P is known to play a critical role in several biochemical pathways involved in the dark phase of photosynthesis, including its involvement in ATP synthesis, NADPH production, and its presence in several key enzymes. Carbon fixation, the initial step in the dark phase of photosynthesis, is a phosphate-driven metabolic process [7].
To minimize the adverse effects of global warming, it is crucial to achieve efficient carbon fixation by increasing vegetation cover and nutrient availability. Baslam et al. highlighted the significant contribution of P in addressing this pressing global challenge, as it impacts the dark phase of photosynthesis directly and indirectly [8]. As global P reserves continue to deplete, it becomes increasingly vital to comprehend the multifaceted role of phosphorus in the dark phase of photosynthesis [9]. In agricultural production, P-deficiency presents a significant limitation, and a better understanding of its contribution to the dark phase of photosynthesis could hold significant implications for improving crop productivity and sustainability [10].
Given above, the goal of this literature review is to provide a detailed understanding of the importance of P in the dark phase of photosynthesis, particularly in the regulation of the CBB cycle and the production of energy-rich molecules, such as ATP and NADPH and its overall significance in the process of photosynthesis.
2. Phosphorus in plant growth and development
Plant growth heavily relies on inorganic nutrients; predominantly N, and P both of which are often limited in the environment, hence these nutrients are frequently administered as fertilizers to plants [11]. An optimal P fertilization can enhance plant biomass yield and improve antioxidant potential [12]. Increasing P-levels can also result in improved growth parameters, including fresh and dry weight, floral number, plant height, and essential oil concentration [13]. Additionally, P plays a crucial role as a metabolic and regulatory nutrient element. However, the interaction of P with other minerals is often stronger than its individual action [14]. Particularly in the dark phase of photosynthesis, the availability of P can significantly impact the efficiency of the CBB cycle and the production of energy-rich molecules such as ATP and NADPH.
P plays a crucial role in enhancing a plant’s ability to resist and tolerate diseases, which can cause significant reductions in both crop yield and quality [15]. Its application is known to enhance plant growth and also to increase resistance to various biotic stresses. For instance, when a pathogen invades a plant, P in the form of ATP is released into the extracellular space, where the plants recognize it as a signal that there is cellular damage [16]. In turn, this signal activates the plant’s defense response to fight off the pathogen. Therefore, ATP is a signaling molecule for the defense response activation in the plant [17]. Further, P-deficiency can have a profound impact on plant growth and productivity, leading to reduced root growth, delayed flowering, impaired seed development, and decreased crop yield [4, 5]. In addition to these direct effects, phosphorus deficiency can also influence the plant’s ability to acquire other essential nutrients, such as N, K, and micronutrients, further exacerbate the impact on plant growth and development [18, 19].
3. Calvin-Benson cycle: An overview
The dark phase of photosynthesis, or the Calvin-Benson cycle, is a series of enzyme-catalyzed reactions that occur in the stroma of chloroplasts [20]. This cycle is responsible for the fixation of CO2 into oces, ultimately producing glucose and other sugars that can be used for various cellular processes [21]. Calvin-Benson cycle consists of three main stages: carboxylation, reduction, and regeneration [22] (Figure 1).
Figure 1.
Calvin–Benson cycle consists of carbon fixation with carbon dioxide, reduction with NADPH and regeneration of the CO2 acceptor. Image adopted from Schreier and Hibberd [
The Calvin cycle, also known as the dark phase of photosynthesis, is a series of enzyme-driven reactions that convert carbon dioxide (CO2) into sugars and other organic molecules. The cycle consists of three main phases: carbon fixation, reduction, and regeneration of the CO2 acceptor molecule ribulose-1,5-bisphosphate (RuBP). During these reactions, P plays a vital role in the form of energy transfer molecules (ATP and NADPH) [23].
3.1 Carboxylation
Carboxylation is the first step of the Calvin-Benson cycle, where CO2 is fixed into an organic molecule through the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) [24]. RuBisCO catalyzes the reaction between CO2 and the five-carbon sugar ribulose-1,5-bisphosphate (RuBP), resulting in two molecules of 3-phosphoglycerate (3-PGA) [25]. The carbon fixation phase begins with the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), which catalyzes the fixation of CO2 to RuBP, producing two molecules of 3-phosphoglycerate (3-PGA) [25]. P is crucial in this step as 3-PGA contains a phosphate group, which is essential for the subsequent steps of the Calvin cycle.
3.2 Reduction
The reduction stage involves the conversion of 3-phosphoglycerate (3-PGA) into glyceraldehyde-3-phosphate (G3P) through two enzyme-catalyzed reactions [26, 27]. First, 3-PGA is phosphorylated by the enzyme phosphoglycerate kinase (PGK), yielding 1,3-bisphosphoglycerate (1,3-BPG) [28]. This reaction requires ATP as a substrate, which is converted into ADP during the process. This step highlights the importance of phosphorus, as ATP is the primary energy currency of the cell and contains a high-energy phosphate bond. Next, glyceraldehyde-3-phosphate dehydrogenase (GAPDH) catalyzes the reduction of 1,3-BPG to G3P, using NADPH as a reducing agent [29]. NADPH, which is another essential molecule containing phosphorus, is generated during the light-dependent reactions of photosynthesis.
3.3 Regeneration
The final stage of the Calvin-Benson cycle is the regeneration of RuBP from G3P [30]. This process involves a series of enzyme-catalyzed reactions that convert the remaining G3P molecules into RuBP. Enzymes involved in this stage include triose phosphate isomerase (TPI), aldolase, fructose-1,6-bisphosphatase (FBPase), transketolase (TK), and sedoheptulose-1,7-bisphosphatase (SBPase) [31]. Transketolase and aldolase are responsible for the interconversion of carbon skeletons between different sugar phosphate molecules, while phosphoribulokinase catalyzes the phosphorylation of ribulose-5-phosphate (Ru5P) to RuBP, utilizing ATP as a phosphate donor. Once again, phosphorus plays a critical role in the form of ATP, providing the energy required for RuBP regeneration. The regenerated RuBP can then be used for another round of carboxylation, continuing the cycle [32].
4. Phosphorus in ATP synthesis and NADPH production
In the dark phase of photosynthesis, P is mainly involved in the synthesis of ATP and the production of NADPH. Both ATP and NADPH are essential energy carriers in the Calvin-Benson cycle, providing the energy and reducing power required for the fixation of CO2 into organic molecules [1].
4.1 ATP synthesis
Adenosine triphosphate (ATP) is a high-energy molecule that serves as the primary energy currency for cells [33]. It is synthesized in the light phase of photosynthesis through a process called photophosphorylation, which occurs in the thylakoid membrane of chloroplasts (Figure 2). During this process, the energy derived from absorbed light is used to pump protons across the thylakoid membrane, creating a proton gradient [35]. The resulting proton motive force drives the synthesis of ATP from ADP and inorganic phosphate (Pi) through the enzyme ATP synthase [36]. P is a critical component of ATP, as it forms the phosphate groups that store and release energy during ATP hydrolysis. High-energy phosphate, held as a part of the chemical structures of adenosine diphosphate (ADP) and ATP, is the source of energy that drives the multitude of chemical reactions within the plant [33]. When ADP and ATP transfer the high-energy phosphate to other molecules (termed phosphorylation), the stage is set for many essential processes to occur.
Figure 2.
Light reactions harness energy from the sun to produce chemical bonds, ATP, and NADPH. Image adopted from [
Several enzymes are involved in the process of ATP synthesis including ATP synthase [37], which according to several studies is sited in the thylakoid membrane of chloroplasts [38, 39, 40]. The activity of ATP synthase, the enzyme responsible for ATP synthesis, is regulated by several factors including the availability of phosphorus [41, 42]. Studies have revealed that P-availability can affect ATP synthesis and cellular energy metabolism. P-deficiency in plants can decrease ATP synthesis and lead to reduced growth and development [9]. This is because P-deficiency inhibits the catalytic activity of ATP synthase, which catalyzes ATP synthesis. Additionally, P-limitation in marine phytoplankton was reported to reduce ATP synthesis [43]. In the dark phase of photosynthesis, ATP is used as an energy source for various enzymatic reactions, such as the phosphorylation of 3-PGA by PGK [44].
4.2 NADPH production
Nicotinamide adenine dinucleotide phosphate (NADPH) is another essential energy carrier in the Calvin-Benson cycle, where it provides reducing power for the conversion of 1,3-BPG to G3P by GAPDH [29]. NADPH is produced during the light phase of photosynthesis in a process called linear electron flow (LEF), which occurs in the thylakoid membrane of chloroplasts [45]. During LEF, electrons are transferred from water molecules to NADP+ through a series of protein complexes and electron carriers, including photosystem II (PSII), the cytochrome b6f complex, photosystem I (PSI), and ferredoxin-NADP+ reductase (FNR) [46]. The reduction of NADP+ to NADPH involves the transfer of two electrons and one proton, with the latter being derived from the hydrolysis of water molecules. P is not directly involved in the production of NADPH, but it is essential for the stability and function of NADP+ and NADPH, as they both contain a phosphate group [47].
5. Phosphorus as a component of ATP and NADPH
ATP and NADPH are two energy-rich molecules that play a central role in the dark phase of photosynthesis (Figure 2). ATP is often referred to as the “energy currency” of the cell, as it can store and release energy in the form of phosphate bonds. In the CBB cycle, ATP provides the energy required for the fixation of CO2 into organic molecules, such as glucose and other sugars. NADPH is an electron carrier that provides the reducing power needed for the synthesis of these organic molecules. Both ATP and NADPH contain phosphate groups, which are essential for their function as energy carriers. In the case of ATP, the molecule consists of three phosphate groups linked to an adenosine molecule. The energy stored in ATP is released when one of the phosphate groups is removed through a process called hydrolysis, resulting in the formation of adenosine diphosphate (ADP) and inorganic phosphate (Pi). This energy can then be used to drive various cellular processes, including the reactions of the CBB cycle [37]. Similarly, NADPH contains a phosphate group as part of its structure. The molecule is derived from its oxidized form, NADP+, by the addition of two electrons and a proton, resulting in the formation of NADPH and the release of a second proton. The reducing power of NADPH is then used in the CBB cycle to convert the fixed CO2 into organic molecules, such as glucose and other sugars [48].
Given the central role of ATP and NADPH in the dark phase of photosynthesis, the availability of P can have a significant impact on the efficiency of the CBB cycle and, consequently, on plant growth and productivity. Indeed, several studies have reported a strong correlation between P-availability and the rate of photosynthesis, with P-deficiency leading to reduced rates of CO2 assimilation and decreased production of ATP and NADPH [49].
6. Phosphorus in key enzymes of the dark phase
Several key enzymes in the Calvin-Benson cycle contain P as a major structural component, highlighting the importance of P in the dark phase of photosynthesis. These enzymes include RuBisCO, PGK, GAPDH, and others involved in the regeneration stage of the cycle [50].
6.1 RuBisCO
RuBisCO, the most abundant enzyme on Earth, is responsible for the carboxylation of RuBP [25]. The enzyme contains a large subunit and a small subunit, both of which are encoded by the chloroplast genome [51]. The large subunit contains a conserved lysine residue that forms a Schiff base with the phosphate group of RuBP, facilitating the binding of CO2 [52]. The active site of RuBisCO also contains a tightly bound Mg2+ ion, which coordinates with the phosphate groups of RuBP and stabilizes the transition state during carboxylation [53].
6.2 PGK and GAPDH
Phosphoribuloseglycerate kinase (PGK) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) are responsible for the phosphorylation and reduction of 3-PGA, respectively [29]. Both enzymes contain P as part of their active sites, with PGK utilizing a phosphohistidine intermediate in its catalytic mechanism, and GAPDH employing a phosphorylated cysteine residue for the transfer of phosphate groups between substrates [29].
6.3 Regeneration enzymes
The regeneration stage of the Calvin-Benson cycle involves several enzymes that are responsible for the recycling of the CO2 acceptor molecule, RuBP, which is essential for the continued fixation of CO2 by the cycle. Some of these enzymes, such as SBPase and FBPase, contain P in their active sites, which play a critical role in their catalytic activity [54]. For example, FBPase uses a phosphohistidine intermediate in its reaction mechanism, while SBPase utilizes a phosphoserine intermediate. Phosphorus is also an integral component of RuBP itself, which is regenerated during this stage of the cycle [27].
7. Phosphorus in the regulation of key enzymes involved in the CBB cycle
The Calvin-Benson-Bassham (CBB) cycle consists of a series of enzyme-catalyzed reactions that assimilate CO2 into organic molecules, such as glucose and other sugars. These reactions can be grouped into three main stages: (1) carboxylation, in which CO2 is fixed to a five-carbon molecule called ribulose-1,5-bisphosphate (RuBP) by the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco); (2) reduction, in which the resulting six-carbon molecule is split into two three-carbon molecules of 3-phosphoglycerate (3-PGA) and subsequently reduced to glyceraldehyde-3-phosphate (G3P) using the energy provided by ATP and NADPH; and (3) regeneration, in which the remaining G3P molecules are used to regenerate RuBP through a series of reactions that also involve the consumption of ATP [55].
P plays a crucial role in the regulation of several key enzymes involved in the CBB cycle, including Rubisco, phosphoribulokinase (PRK), and GAPDH. For example, Rubisco, the most abundant enzyme in the chloroplast and responsible for the carboxylation of RuBP, requires a divalent metal ion, such as Mg2+, for its catalytic activity [56]. In the dark, the Mg2+ ion is replaced by a proton, leading to the formation of a stable complex between Rubisco and a molecule of RuBP. The addition of inorganic phosphate (Pi) can reverse this inhibition by promoting the release of the proton and the re-activation of the enzyme [57]. Therefore, the activity of RuBisCO is regulated by the phosphorylation and dephosphorylation of its activase, RuBisCO activase [58]. The phosphorylation status of RuBisCO activase is modulated by a protein kinase and a phosphatase, which are sensitive to the ATP/ADP ratio in the chloroplast stroma [58]. This regulation ensures that RuBisCO activity is adjusted according to the energy availability within the cell.
Similarly, PRK, the enzyme responsible for the phosphorylation of ribulose-5-phosphate (Ru5P) to RuBP, is also regulated by the availability of Pi. The enzyme is inhibited by the binding of a molecule of ADP, which competes with the substrate, ATP, for the same binding site. The addition of Pi can relieve this inhibition by promoting the formation of ATP from ADP and Pi, thereby allowing the enzyme to resume its catalytic activity [27, 59]. Finally, GAPDH, the enzyme that catalyzes the reduction of 1,3-bisphosphoglycerate (1,3-BPG) to G3P using NADPH as the reducing agent, is also sensitive to changes in the availability of Pi. The enzyme forms a complex with another enzyme, phosphoribuloseglycerate kinase (PGK), and the two enzymes work together in a coupled reaction to convert 3-PGA to G3P. The formation of this complex is dependent on the presence of Pi, which acts as a stabilizing factor and ensures the efficient transfer of phosphate groups between the two enzymes [60, 61].
8. Phosphorus and photosynthetic efficiency
The efficient functioning of the dark phase of photosynthesis is directly impacted by the availability of P, a vital component in the production of energy transfer molecules ATP and NADPH [9, 62]. Without sufficient P, plants cannot produce these molecules, leading to reduced photosynthesis and decreased crop yields. Several studies have shown the importance of P in photosynthesis and crop productivity. For example, P-deficiency can significantly reduce the photosynthetic rate and yield [63]. Similarly, P-deficient soils can negatively impact the growth and yield of teff, a staple crop in Ethiopia [64]. Moreover, P-deficiency can also lead to a decrease in the activity of key enzymes involved in the Calvin cycle, such as RuBisCO, further contributing to the reduction in photosynthetic efficiency [65]. Being a key component of ADP and ATP synthase P is required for optimal photosynthetic activity. Hence, P-deficiency limits or halts the biochemical process of phosphorylation and limits the catalytic activity of energy-producing enzymes [66, 67].
Unfortunately, P is often limited in soils, making it a scarce resource for plants. Excessive use of P-fertilizers can also lead to environmental problems. The over-application of P-fertilizers, surpassing crop demand, poses a heightened risk of P-loss from soil to water resources and can result in the degradation of water quality through eutrophication [68]. Therefore, it is important for farmers to understand how to manage phosphorus effectively in their soils to ensure sustainable crop production. One approach to managing P effectively is using precision agriculture techniques. For example, a study conducted in Ghana showed that precision application of P-fertilizer based on soil testing and yield potential resulted in higher crop yields and reduced phosphorus runoff compared to traditional broadcasting of fertilizer [69]. In response to P-deficiency, plants can develop adaptive mechanisms, such as increasing the expression of high-affinity phosphate transporters and enhancing the secretion of acid phosphatases, which help to increase phosphorus uptake and utilization [70]. Plants also modify their metabolic pathways and root morphology, and this involves changes in their gene expression. A range of proteins involved in the various metabolic pathways are differentially expressed in response to phosphate stress, suggesting that they may play important roles in regulating complex adaptation activities for Pi deprivation to facilitate P-homeostasis [71]. The proteins that respond to P shortage may be involved in various processes including phytohormone biosynthesis, signal transduction, cellular organization and defense, and energy and carbon metabolism [72]. These proteins are likely to play a crucial role in sensing the changes in external Pi concentration and regulating complex adaptation activities that enable plants to maintain P homeostasis.
9. Conclusions and future perspective
P has been widely known to play a crucial role in the dark phase of photosynthesis, particularly in the Calvin cycle. It is involved in the formation of essential molecules like ATP, NADPH, and sugar phosphates, which are indispensable for the carbon fixation, reduction, and regeneration of RuBP. Additionally, phosphorus is involved in the regulation of key enzymes, such as RuBisCO, through the modulation of its activase. P-availability can directly impact the efficiency of the dark phase of photosynthesis, with P- deficiency leading to reduced photosynthetic rates and adaptive responses in plants. Understanding the role of P in the dark phase of photosynthesis is vital for improving crop productivity and developing sustainable agricultural practices. Future research should focus on identifying novel strategies to enhance P-use efficiency in plants, as well as exploring the potential interactions between phosphorus and other nutrients, such as N and K, in the regulation of photosynthetic processes.
Acknowledgments
The authors would like to express gratitude to all the national service personnel of the 2022 group at the Department of Medical Microbiology, University of Ghana Medical School, for their invaluable assistance and contributions to this project.
Conflict of interest
The authors declare no conflict of interest.
Appendices and nomenclature
3 -phosphoglycerate | |
Adenosine triphosphate | |
Nicotinamide adenine dinucleotide phosphate | |
inorganic phosphate | |
organic phosphate | |
Ribulose-1, 5-bisphosphate carboxylase-oxygenase | |
ribulose-1-5-bisphosphate | |
Calvin-Benson-Bassham |
References
- 1.
Johnson MP. Photosynthesis. Essays Biochemical. 2016; 60 (3):255-273 Available from:https://pubmed.ncbi.nlm.nih.gov/27784776 - 2.
Janssen PJD, Lambreva MD, Plumeré N, Bartolucci C, Antonacci A, Buonasera K, et al. Photosynthesis at the forefront of a sustainable life. Frontier in Chemistry. 2014; 2 :36. Available from:https://pubmed.ncbi.nlm.nih.gov/24971306 - 3.
Trinh MDL, Masuda S. Chloroplast pH homeostasis for the regulation of photosynthesis. Frontier in Plant Science. 2022; 13 :919896. Available from:https://pubmed.ncbi.nlm.nih.gov/35693183 - 4.
Vance CP, Uhde-Stone C, Allan DL. Phosphorus acquisition and use: Critical adaptations by plants for securing a nonrenewable resource. New Phytologist. 2003; 157 (3):423-447. DOI: 10.1046/j.1469-8137.2003.00695.x - 5.
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, et al. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist. 2012; 195 (2):306-320. DOI: 10.1111/j.1469-8137.2012.04190.x - 6.
Raghothama KG. Phosphate acquisition. Annual Review in Plant Physiology Plant Molecular Biology. 1999; 50 (1):665-693. DOI: 10.1146/annurev.arplant.50.1.665 - 7.
Stirbet A, Lazár D, Guo Y, Govindjee G. Photosynthesis: Basics, history and modelling. Annals of Botany. 2020; 126 (4):511-537. Available from:https://pubmed.ncbi.nlm.nih.gov/31641747 - 8.
Baslam M, Mitsui T, Hodges M, Priesack E, Herritt MT, Aranjuelo I, et al. Photosynthesis in a changing global climate: Scaling up and scaling down in crops. Frontier in Plant Science. 2020; 11 :882. Available from:https://pubmed.ncbi.nlm.nih.gov/32733499 - 9.
Carstensen A, Herdean A, Schmidt SB, Sharma A, Spetea C, Pribil M, et al. The impacts of phosphorus deficiency on the photosynthetic electron transport chain. Plant Physiology. 2018; 177 (1):271-284 Available from:https://pubmed.ncbi.nlm.nih.gov/29540590 - 10.
Bechtaoui N, Rabiu MK, Raklami A, Oufdou K, Hafidi M, Jemo M. Phosphate-dependent regulation of growth and stresses management in plants. Frontier in Plant Science. 2021; 12 :679916. Available from:https://pubmed.ncbi.nlm.nih.gov/34777404 - 11.
Guignard MS, Leitch AR, Acquisti C, Eizaguirre C, Elser JJ, Hessen DO, et al. Impacts of nitrogen and phosphorus: From genomes to natural ecosystems and agriculture. Frontier in Ecology Evolution. 2017; 2017 :5. DOI: 10.3389/fevo.2017.00070 - 12.
Nell M, Vötsch M, Vierheilig H, Steinkellner S, Zitterl-Eglseer K, Franz C, et al. Effect of phosphorus uptake on growth and secondary metabolites of garden sage ( Salvia officinalis L.). Journal of Science Food Agriculture. 2009;89 (6):1090-1096. DOI: 10.1002/jsfa.3561 - 13.
Chrysargyris A, Panayiotou C, Tzortzakis N. Nitrogen and phosphorus levels affected plant growth, essential oil composition and antioxidant status of lavender plant ( Lavandula angustifolia Mill.). Industrial Crops Products. 2016;83 :577-586. DOI: 10.1016/j.indcrop.2015.12.067 - 14.
Wu W, Zhu S, Chen Q , Lin Y, Tian J, Liang C. Cell Wall proteins play critical roles in plant adaptation to phosphorus deficiency. International Journal of Molecular Science. 2009; 20 (21):5259 Available from:https://pubmed.ncbi.nlm.nih.gov/31652783 - 15.
Ainsworth EA, Long SP. 30 years of free-air carbon dioxide enrichment (FACE): What have we learned about future crop productivity and its potential for adaptation? Global Change Biology. 2020; 27 (1):27-49. DOI: 10.1111/gcb.15375 - 16.
Kumar S, Tripathi D, Okubara PA, Tanaka K. Purinoceptor P2K1/DORN1 enhances plant resistance against a Soilborne fungal pathogen, Rhizoctonia solani . Frontier in Plant Science. 2020;11 :572920. Available from:https://pubmed.ncbi.nlm.nih.gov/33101341 - 17.
Tripathi D, Zhang T, Koo AJ, Stacey G, Tanaka K. Extracellular ATP acts on Jasmonate Signaling to reinforce plant Defense. Plant Physiology. 2017; 176 (1):511-523. Available from:https://pubmed.ncbi.nlm.nih.gov/29180381 - 18.
Hermans C, Hammond JP, White PJ, Verbruggen N. How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science. 2006; 11 (12):610-617. DOI: 10.1016/j.tplants.2006.10.007 - 19.
Lambers H, Raven J, Shaver G, Smith S. Plant nutrient-acquisition strategies change with soil age. Trends in Ecology & Evolution. 2008; 23 (2):95-103. DOI: 10.1016/j.tree.2007.10.008 - 20.
Calvin M, Benson AA. The path of carbon in photosynthesis. Science (1979). 1948; 107 (2784):476-480. DOI: 10.1126/science.107.2784.476 - 21.
Zhu XG, Long SP, Ort DR. What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Current Opinion in Biotechnology. 2008; 19 (2):153-159. DOI: 10.1016/j.copbio.2008.02.004 - 22.
Schreier TB, Hibberd JM. Variations in the Calvin-Benson cycle: Selection pressures and optimization? Journal of Experimental Botany. 2019; 70 (6):1697-1701. Available from:https://pubmed.ncbi.nlm.nih.gov/30916343 - 23.
Bassham JA, Krause GH. Free energy changes and metabolic regulation in steady-state photosynthetic carbon reduction. Biochimica et Biophysica Acta (BBA) – Bioenergetics. 1969; 189 (2):207-221. DOI: 10.1016/0005-2728(69)90048-6 - 24.
Whitmarsh J, Govindjee. Photosynthesis. In: Digital Encyclopedia of Applied Physics. 2003. DOI: 10.1002/3527600434.eap327 - 25.
Spreitzer RJ, Salvucci ME. RUBISCO: Structure, Regulatory interactions, and possibilities for a better enzyme. Annual Review in Plant Biology. 2002; 53 (1):449-475. DOI: 10.1146/annurev.arplant.53.100301.135233 - 26.
Johnson X, Alric J. Central carbon metabolism and electron transport in Chlamydomonas reinhardtii : Metabolic constraints for carbon partitioning between oil and starch. Eukaryotic Cell. 2013;12 (6):776-793. Available from:https://pubmed.ncbi.nlm.nih.gov/23543671 - 27.
Meloni M, Gurrieri L, Fermani S, Velie L, Sparla F, Crozet P, et al. Ribulose-1,5-bisphosphate regeneration in the Calvin-Benson-Bassham cycle: Focus on the last three enzymatic steps that allow the formation of Rubisco substrate. Frontier in Plant Science. 2023; 14 :1130430. Available from:https://pubmed.ncbi.nlm.nih.gov/3687559 - 28.
Rosa-Téllez S, Anoman AD, Flores-Tornero M, Toujani W, Alseek S, Fernie AR, et al. Phosphoglycerate kinases are Co-regulated to adjust metabolism and to optimize growth. Plant Physiology. 2017; 176 (2):1182-1198. Available from:https://pubmed.ncbi.nlm.nih.gov/28951489 - 29.
Zaffagnini M, Bedhomme M, Groni H, Marchand CH, Puppo C, Gontero B, et al. Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: A proteomic survey. Molecular Cell Proteomics. 2011; 11 (2):M111.014142-M111.014142. Available from:https://pubmed.ncbi.nlm.nih.gov/22122882 - 30.
Yamaoka C, Suzuki Y, Makino A. Differential expression of genes of the Calvin–Benson cycle and its related genes during leaf development in rice. Plant Cell Physiology. 2015; 57 (1):115-124. DOI: 10.1093/pcp/pcv183 - 31.
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL. Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment. 2007; 30 (9):1035-1040. DOI: 10.1111/j.1365-3040.2007.01710.x - 32.
Cen YP, Sage RF. The regulation of Rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiology. 2005; 139 (2):979-990. Available from:https://pubmed.ncbi.nlm.nih.gov/16183840 - 33.
Pinna S, Kunz C, Halpern A, Harrison SA, Jordan SF, Ward J, et al. A prebiotic basis for ATP as the universal energy currency. PLoS Biology. 2022; 20 (10):e3001437-e3001437. Available from:https://pubmed.ncbi.nlm.nih.gov/36194581 - 34.
Biology, The Cell, Photosynthesis, using Light Energy to Make Organic Molecules. VIVA Open. 2023. Available from: https://vivaopen.oercommons.org/courseware/lesson/474/overview - 35.
Blankenship RE. Molecular Mechanisms of Photosynthesis. Wiley; 2002. DOI: 10.1002/9780470758472 - 36.
Nelson N, Ben-Shem A. The complex architecture of oxygenic photosynthesis. Natural Review in Molecular Cell Biology. 2004; 5 (12):971-982. DOI: 10.1038/nrm1525 - 37.
Bonora M, Patergnani S, Rimessi A, De Marchi E, Suski JM, Bononi A, et al. ATP synthesis and storage. Purinergic Signaling. 2012; 8 (3):343-357. Available from:https://pubmed.ncbi.nlm.nih.gov/22528680 - 38.
Neupane P, Bhuju S, Thapa N, Bhattarai HK. ATP synthase: Structure, function and inhibition. Biomolecular Concepts. 2019; 10 (1):1-10. DOI: 10.1515/bmc-2019-0001 - 39.
Kaim G, Dimroth P. ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO Journal. 1999; 18 (15):4118-4127 Available from:https://pubmed.ncbi.nlm.nih.gov/10428951 - 40.
Daum B, Nicastro D, Austin J 2nd, McIntosh JR, Kühlbrandt W. Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell. 2010; 22 (4):1299-1312. Available from:https://pubmed.ncbi.nlm.nih.gov/20388855 - 41.
Kühlbrandt W. Structure and function of mitochondrial membrane protein complexes. BMC Biology. 2015; 13 :89. Available from:https://pubmed.ncbi.nlm.nih.gov/26515107 - 42.
Igamberdiev AU, Kleczkowski LA. Optimization of ATP synthase function in mitochondria and chloroplasts via the adenylate kinase equilibrium. Frontier in Plant Science. 2015; 6 :10. Available from:https://pubmed.ncbi.nlm.nih.gov/25674099 - 43.
Feng TY, Yang ZK, Zheng JW, Xie Y, Li DW, Murugan SB, et al. Examination of metabolic responses to phosphorus limitation via proteomic analyses in the marine diatom Phaeodactylum tricornutum. Scientific Reports. 2015; 5 :10373. Available from:https://pubmed.ncbi.nlm.nih.gov/26020491 - 44.
Scheibe R. Maintaining homeostasis by controlled alternatives for energy distribution in plant cells under changing conditions of supply and demand. Photosynthetic Research. 2018; 139 (1-3):81-91. Available from:https://pubmed.ncbi.nlm.nih.gov/30203365 - 45.
Nikkanen L, Toivola J, Trotta A, Diaz MG, Tikkanen M, Aro EM, et al. Regulation of cyclic electron flow by chloroplast NADPH-dependent thioredoxin system. Plant Direction. 2018; 2 :11, e00093-e00093. Available from:https://pubmed.ncbi.nlm.nih.gov/31245694 - 46.
Mulo P. Chloroplast-targeted ferredoxin-NADP+ oxidoreductase (FNR): Structure, function and location. Biochimica et Biophysica Acta (BBA) – Bioenergetics. 2011; 1807 (8):927-934. DOI: 10.1016/j.bbabio.2010.10.001 - 47.
Pollak N, Dölle C, Ziegler M. The power to reduce: pyridine nucleotides--small molecules with a multitude of functions. Biochemical Journal. 2007; 402 (2):205-218. Available from:https://pubmed.ncbi.nlm.nih.gov/17295611 - 48.
Saint-Sorny M, Brzezowski P, Arrivault S, Alric J, Johnson X. Interactions between carbon metabolism and photosynthetic electron transport in a Chlamydomonas reinhardtii mutant without CO(2) fixation by RuBisCO. Frontier in Plant Science. 2022;13 :876439. Available from:https://pubmed.ncbi.nlm.nih.gov/35574084 - 49.
Jacob J, Lawlor DW. Dependence of photosynthesis of sunflower and maize leaves on phosphate supply, ribulose-1,5-bisphosphate carboxylase/oxygenase activity, and ribulose-1,5-bisphosphate pool size. Plant Physiology. 1992; 98 (3):801-807. Available from:https://pubmed.ncbi.nlm.nih.gov/16668751 - 50.
Mettler T, Mühlhaus T, Hemme D, Schöttler MA, Rupprecht J, Idoine A, et al. Systems analysis of the response of photosynthesis, metabolism, and growth to an increase in irradiance in the photosynthetic model organism Chlamydomonas reinhardtii . Plant Cell. 2014;26 (6):2310-2350. Available from:https://pubmed.ncbi.nlm.nih.gov/24894045 - 51.
Yamori W, Hikosaka K, Way DA. Temperature response of photosynthesis in C3, C4, and CAM plants: Temperature acclimation and temperature adaptation. Photosynthetic Research. 2013; 119 (1-2):101-117. DOI: 10.1007/s11120-013-9874-6 - 52.
Andersson I, Backlund A. Structure and function of Rubisco. Plant Physiology and Biochemistry. 2008; 46 (3):275-291. DOI: 10.1016/j.plaphy.2008.01.001 - 53.
Lorimer GH. The carboxylation and oxygenation of ribulose 1,5-bisphosphate: The primary events in photosynthesis and photorespiration. Annual Review in Plant Physiology. 1981; 32 (1):349-382. DOI: 10.1146/annurev.pp.32.060181.002025 - 54.
Raines CA. Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: Current and future strategies. Plant Physiology. 2010; 155 (1):36-42. Available from:https://pubmed.ncbi.nlm.nih.gov/21071599 - 55.
Bassham JA, Calvin M. The way of CO2 in plant photosynthesis. Comparative Biochemistry and Physiology. 1962; 4 :187-204. DOI: 10.1016/0010-406X(62)90004-X - 56.
Portis AR, Parry MAJ. Discoveries in Rubisco (Ribulose 1,5-bisphosphate carboxylase/oxygenase): A historical perspective. Photosynthetic Research. 2007; 94 (1):121-143. DOI: 10.1007/s11120-007-9225-6 - 57.
Erb TJ, Zarzycki J. A short history of RubisCO: The rise and fall (?) of Nature’s predominant CO(2) fixing enzyme. Current Opinion in Biotechnology. 2017; 49 :100-107. Available from:https://pubmed.ncbi.nlm.nih.gov/28843191 - 58.
Portis AR Jr. The rubisco Activase-rubisco system: An ATPase-dependent association that regulates photosynthesis. In: Annual Plant Reviews Book Series, Volume 7: Protein-Protein Interactions in Plant Biology. John Wiley & Sons, Ltd; 2018. pp. 245-259. DOI: 10.1002/9781119312994.apr0057 - 59.
Hammond ET, Andrews TJ, Woodrow IE. Regulation of ribulose-1,5-bisphosphate Carboxylase/Oxygenase by carbamylation and 2-carboxyarabinitol 1-phosphate in tobacco: Insights from studies of antisense plants containing reduced amounts of rubisco activase. Plant Physiology. 1998; 118 (4):1463-1471. Available from:https://pubmed.ncbi.nlm.nih.gov/9847122 - 60.
Scheibe R. Malate valves to balance cellular energy supply. Physiology Plant. 2004; 120 (1):21-26. DOI: 10.1111/j.0031-9317.2004.0222.x - 61.
Wedel N, Soll J. Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/ glyceraldehyde-3-phosphate dehydrogenase complex dissociation. Proceedings of thee National Academy Science USA. 1998; 95 (16):9699-9704. Available from:https://pubmed.ncbi.nlm.nih.gov/9689144 - 62.
Foyer CH, Lopez-Delgado H, Dat JF, Scott IM. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiology Plant. 1997; 100 (2):241-254. DOI: 10.1034/j.1399-3054.1997.1000205.x - 63.
Meng X, Chen WW, Wang YY, Huang ZR, Ye X, Chen LS, et al. Effects of phosphorus deficiency on the absorption of mineral nutrients, photosynthetic system performance and antioxidant metabolism in Citrus grandis . PLoS One. 2021;16 (2):e0246944-e0246944. Available from:https://pubmed.ncbi.nlm.nih.gov/33596244 - 64.
Mihretie FA, Tsunekawa A, Haregeweyn N, Adgo E, Tsubo M, Masunaga T, et al. Exploring teff yield variability related with farm management and soil property in contrasting agro-ecologies in Ethiopia. Agricultural System. 2022; 196 :103338. DOI: 10.1016/j.agsy.2021.103338 - 65.
Strand A, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P, et al. Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiology. 1999; 119 (4):1398-1387. Available from:https://pubmed.ncbi.nlm.nih.gov/10198098 - 66.
Lawlor DW. Limitation to photosynthesis in water-stressed leaves: Stomata vs. metabolism and the role of ATP. Annals of Botany. 2002; 89 (7):885-871. Available from:https://pubmed.ncbi.nlm.nih.gov/12102513 - 67.
de Bang TC, Husted S, Laursen KH, Persson DP, Schjoerring JK. The molecular–physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants. New Phytologist. 2020; 229 (5):2446-2469. DOI: 10.1111/nph.17074 - 68.
von Wandruszka R. Phosphorus retention in calcareous soils and the effect of organic matter on its mobility. Geochemical Transaction. 2006; 7 :6. Available from:https://pubmed.ncbi.nlm.nih.gov/16768791 - 69.
Adjei-Nsiah S, Alabi BU, Ahiakpa JK, Kanampiu F. Response of grain legumes to phosphorus application in the Guinea Savanna agro-ecological zones of Ghana. Agron Journal. 2018; 110 (3):1089-1096 Available from:https://pubmed.ncbi.nlm.nih.gov/33281193 - 70.
Mehra P, Pandey BK, Giri J. Improvement in phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnological Journal. 2017; 15 (8):1054-1067. Available from:https://pubmed.ncbi.nlm.nih.gov/28116829 - 71.
Srivastava S, Ranjan M, Bano N, Asif MH, Srivastava S. Comparative transcriptome analysis reveals the phosphate starvation alleviation mechanism of phosphate accumulating Pseudomonas putida inArabidopsis thaliana . Scientific Report. 2023;13 (1):4918. Available from:https://pubmed.ncbi.nlm.nih.gov/36966146 - 72.
Finkelstein R. Abscisic acid synthesis and response. Arabidopsis Book. 2013; 1 (11):e0166-e0166. Available from:https://pubmed.ncbi.nlm.nih.gov/24273463