1 Introduction

Photosynthesis is a fundamental biological process that converts solar energy into chemical energy, fueling almost all life on Earth. This process involves the absorption of light, the transfer of excitation energy to reaction centers, primary photochemistry, electron and proton transport, ATP synthesis, and CO₂ fixation through the Calvin-Benson cycle and the Hatch-Slack cycle (Stirbet et al., 2019). Photosynthetic organisms, including plants, algae, and cyanobacteria, utilize a sophisticated apparatus to split water and transport electrons to high-energy electron acceptors, balancing energy harvesting and utilization to prevent cellular damage (Lima-Melo et al., 2021). The efficiency of photosynthesis is crucial for plant growth and productivity, and it is influenced by various factors, including light intensity, wavelength, and environmental conditions (Chen et al., 2018).

Maize (Zea mays L.), also known as corn, is one of the most important cereal crops globally, serving as a staple food for millions of people and a critical feedstock for livestock (Zhou and Xu, 2024). Understanding the photosynthetic machinery of maize is essential for improving its productivity and resilience to environmental stresses. Photosynthesis in maize, a C₄ plant, involves unique mechanisms that enhance its efficiency, such as the spatial separation of initial CO₂ fixation and the Calvin cycle, which reduces photorespiration (Li et al., 2023a). Research has shown that optimizing photosynthetic efficiency can significantly increase crop yields and help mitigate the impacts of climate change (Liu et al., 2019; Li et al., 2023). Additionally, studies on the interaction between maize and nanomaterials have revealed potential strategies to enhance photosynthesis and growth through metabolic reprogramming (Li et al., 2020a).

This study provides a comprehensive understanding of the molecular mechanisms underlying the photosynthetic machinery in maize. This includes examining the roles of key components such as Photosystem I (PSI) and Photosystem II (PSII), the regulation and protection of these systems under fluctuating environmental conditions, and the potential for bioengineering to enhance photosynthetic efficiency. By synthesizing current research findings, this study aims to identify knowledge gaps and propose future research directions to improve maize photosynthesis and, consequently, its agricultural productivity.

2 Photosynthetic Machinery in Maize

2.1 Structure and function of photosynthetic components

The photosynthetic machinery in maize, like in other plants, is located within the thylakoid membranes of chloroplasts. This machinery is responsible for converting light energy into chemical energy through a series of complex processes. The primary components include Photosystems I and II (PSI and PSII), light-harvesting complexes (LHCs), the electron transport chain, and ATP synthase. These components work together to capture light energy, transfer electrons, and synthesize ATP and NADPH, which are essential for the Calvin cycle and other metabolic processes.

2.2 Photosystems I and II: composition and roles

Photosystem I (PSI) and Photosystem II (PSII) are integral to the photosynthetic process. PSI is composed of multiple subunits, including a core complex and light-harvesting complexes (LHCI). In maize, PSI can form super complexes with LHCI and LHCII, which help in balancing energy flow under fluctuating light conditions (Pan et al., 2018). PSII, on the other hand, is primarily responsible for the initial capture of light energy and the splitting of water molecules to release oxygen. Both photosystems work in tandem to drive the linear electron flow, which is crucial for the production of ATP and NADPH (Pan et al., 2018; Crepin et al., 2019).

2.3 Light Harvesting Complexes (LHC) and their function

Light-harvesting complexes (LHCs) are essential for capturing light energy and transferring it to the reaction centers of PSI and PSII. In maize, LHCs are composed of chlorophylls and carotenoids bound to specific proteins. These complexes not only increase the absorption cross-section of the photosystems but also play a critical role in photoprotection by dissipating excess light energy (Lokstein et al., 2021; Wang et al., 2021). The trimeric LHCII is the main antenna complex of PSII, and its phosphorylation state can influence its association with PSI, thereby optimizing energy distribution between the photosystems (Pan et al., 2018; Vayghan et al., 2021).

2.4 Electron transport chain and atp synthesis

The electron transport chain (ETC) in maize involves a series of protein complexes and mobile electron carriers that facilitate the transfer of electrons from PSII to PSI. This process generates a proton gradient across the thylakoid membrane, which drives ATP synthesis through ATP synthase. The ETC includes components such as cytochrome b6f complex, plastoquinone, and plastocyanin. Additionally, cyclic electron flow around PSI can occur, which helps in generating additional ATP without the production of NADPH, thus balancing the ATP/NADPH ratio required for the Calvin cycle (Steinbeck et al., 2018).

2.5 Carbon fixation pathways (C₃, C₄, CAM) and their relevance to maize

Maize utilizes the C₄ carbon fixation pathway, which is highly efficient in hot and dry environments. This pathway involves the initial fixation of CO₂ into a four-carbon compound, oxaloacetate, which is then converted into malate. Malate is transported to bundle-sheath cells, where it releases CO₂ for the Calvin cycle. This mechanism minimizes photorespiration and enhances water-use efficiency, making maize well-suited for growth in arid conditions. The C₄ pathway is a significant evolutionary adaptation that allows maize to maintain high photosynthetic efficiency under stress conditions (Jang and Mennucci, 2018).

By understanding the intricate details of the photosynthetic machinery in maize, researchers can explore ways to enhance crop productivity and stress tolerance, which are crucial for meeting the growing global food demand.

3 Molecular Regulation of Photosynthesis in Maize

3.1 Gene expression profiles underlying photosynthesis

The gene expression profiles underlying photosynthesis in maize are complex and involve the coordinated expression of numerous genes. Single-cell RNA sequencing (scRNA-seq) has revealed that various transcription factor (TF) families, such as WRKY, ERF, NAC, MYB, and Heat stress transcription factors (HSF), play significant roles in the early stages of mesophyll cell development, which is crucial for photosynthesis (Figure 1) (Tao et al., 2022). Additionally, the compartmentation of photosynthesis gene expression in maize is influenced by the time of day, with peak expression of C₄ cycle genes occurring between 6 and 10 hours after dawn, coinciding with maximum photosynthetic rates (Borba et al., 2023).

Figure 1  Single-Cell RNA sequencing analysis of maize leaf cells (Adapted from Tao et al., 2022) Image caption: (A) UMAP-based scatterplot displaying eight distinct cell clusters identified from 7,354 filtered maize leaf cells. (B) Dot plot illustrating the average expression levels of 16 genes specific to various cell types, differentially expressed between mesophyll (M) cells, bundle sheath (BS) cells, and other cell types across the eight Seurat clusters. The dot size indicates the proportion of cells expressing each gene, with genes more highly expressed in BS cells highlighted on a grey background. (C) Scatter plot comparing log2 (mean RPM+1) values for all genes in bulk RNA-seq data (x-axis) and scRNA-seq data (y-axis), with each dot's color representing the log2-transformed number of cells expressing the gene in the scRNA-seq. The correlation between the two datasets was assessed using the Spearman correlation test (Adapted from Tao et al., 2022)

3.2 Regulation by light and circadian rhythms

Light and circadian rhythms are critical regulators of photosynthesis in maize. The expression of photosynthesis-related genes is tightly regulated by light intensity and circadian rhythms, with maximal photosynthetic activity observed around midday (Borba et al., 2023). Light exposure significantly inhibits the elongation of maize mesocotyl and coleoptile by modulating phytohormone levels and lignin deposition, which in turn affects the expression of genes involved in circadian rhythm and phytohormone biosynthesis (Zhao et al., 2023).

3.3 Role of transcription factors and gene networks

Transcription factors (TFs) play pivotal roles in regulating photosynthesis in maize. For instance, basic Helix-Loop-Helix (bHLH) TFs, such as ZmbHLH128 and ZmbHLH129, bind to the promoter of the NADP-Malic Enzyme (NADP-ME) gene, a key enzyme in C₄ photosynthesis, indicating the importance of TFs in the regulation of photosynthetic genes (Borba et al., 2018). Moreover, the construction of gene regulatory networks has identified several TF families, including DOF and MADS-domain TFs, as key regulators of diurnal fluctuations in C4 gene expression (Borba et al., 2023). The integration of transcriptome data with TF binding motifs has further elucidated the complex regulatory networks controlling photosynthesis (Dai et al., 2021).

3.4 Post-translational modifications and their impact on photosynthetic efficiency

Post-translational modifications (PTMs) significantly impact photosynthetic efficiency in maize. Although the detailed mechanisms of PTMs in photosynthesis are not fully understood, it is known that PTMs can modulate the activity of photosynthetic proteins and enzymes, thereby influencing overall photosynthetic performance. For example, the regulation of photosynthesis by transcription factors often involves PTMs that affect their stability, localization, and interaction with other proteins (Halpape et al., 2023).

3.5 Impact of epigenetic modifications on photosynthetic genes

Epigenetic modifications, such as DNA methylation and histone modifications, play crucial roles in the regulation of photosynthetic genes in maize. Chromatin accessibility and epigenetic features, including H3K27me3 modification and CHH methylation, coordinate to regulate cell type-specific gene expression in bundle sheath and mesophyll cells (Dai et al., 2021). These epigenetic modifications ensure the proper expression of key C₄ genes, thereby optimizing photosynthetic efficiency. Additionally, the integration of epigenetic data with gene expression profiles has identified potential key C₄ genes and provided insights into the regulatory mechanisms of C₄ photosynthesis (Dai et al., 2021).

In summary, the molecular regulation of photosynthesis in maize involves a complex interplay of gene expression profiles, light and circadian rhythms, transcription factors, post-translational modifications, and epigenetic modifications. Understanding these regulatory mechanisms is essential for improving photosynthetic efficiency and crop productivity.

4 Genetic and Biotechnological Approaches to Enhancing Photosynthesis in Maize

4.1 Genetic variability in photosynthetic traits in maize

Genetic variability in photosynthetic traits is a crucial factor for improving maize yield and resilience. Large germplasm collections, including historical collections of crop species and their wild relatives, offer a wealth of opportunities to find novel allelic variations in key photosynthetic processes. These genetic resources can be selectively targeted to enhance photosynthetic efficiency through modern breeding programs (Figure 2) (Sharwood et al., 2022). Additionally, genome-wide association studies (GWAS) have identified significant genetic variations in photosynthesis-related traits, such as leaf net photosynthesis and stomatal conductance, which are promising targets for breeding programs (Yi et al., 2023).

Figure 2 Exploring photosynthetic pathways for enhanced crop yield and future improvement strategies (Adapted from Sharwood et al., 2022) Image caption: The key photosynthetic components-light reactions, CO2 fixation, and photorespiration that contribute to crop yield. Recent gene technology advancements have identified several targets for improving these processes. Enhancements include increasing electron transport for the Calvin cycle by modifying Cyt b6f levels, optimizing Rubisco activity through catalytic alterations, and engineering thermotolerant Rubisco activase for better performance at elevated temperatures. Ambitious strategies like introducing CO2-concentrating mechanisms (CCMs) such as the C4 CCM, carboxysomes, or pyrenoids into crops are also explored. Additional opportunities involve improving CO2 diffusion, Calvin cycle flux, sugar signaling, and altering the photorespiratory pathway to boost plant productivity. These innovations present potential pathways for future-proofing crop productivity in response to environmental challenges (Adapted from Sharwood et al., 2022)

4.2 Molecular breeding for improved photosynthetic efficiency

Molecular breeding techniques, including genomic selection and marker-assisted selection, have been employed to enhance photosynthetic efficiency in maize. The integration of high-throughput phenotyping with genomic data allows for the dissection of complex traits and the identification of novel genes associated with photosynthesis. This approach facilitates the development of maize cultivars with improved photosynthetic efficiency and yield potential (Bezouw et al., 2019). The use of quantitative trait loci (QTL) mapping has also been instrumental in identifying minor QTLs associated with photosynthesis-related traits, providing valuable targets for molecular breeding (Yi et al., 2023).

4.3 CRISPR-Cas9 and other gene editing techniques

CRISPR-Cas9 has emerged as a powerful tool for precise genome editing in maize, enabling targeted deletions, additions, and corrections in the genome. This technology has been successfully applied to edit multiple genes associated with agronomic traits, including photosynthesis. For instance, high-throughput CRISPR/Cas9 mutagenesis has streamlined trait gene identification, allowing for the rapid validation of important agronomic genes (Liu et al., 2020). Additionally, promoter editing of CLE genes using CRISPR-Cas9 has engineered quantitative variation for yield-related traits, demonstrating the potential of this technology in crop enhancement (Liu et al., 2021). The development of multiplex genome editing strategies, such as BREEDIT, further accelerates the improvement of complex traits by targeting multiple genes simultaneously (Lorenzo et al., 2022).

4.4 Transgenic approaches and their successes

Transgenic approaches have been employed to introduce foreign genes into maize to enhance photosynthetic efficiency and yield. These approaches have led to the development of maize varieties with improved stress tolerance, higher yield, and better photosynthetic performance. For example, the integration of CRISPR/Cas9 with transgenic techniques has facilitated the creation of novel maize germplasms with enhanced traits (Wang et al., 2022). The use of haploid-inducer mediated genome editing has also accelerated the breeding process by generating homozygous pure lines with desired traits within two generations (Wang et al., 2019).

4.5 Challenges and future directions in photosynthesis enhancement

Despite the advancements in genetic and biotechnological approaches, several challenges remain in enhancing photosynthesis in maize. The complex genetic architecture of photosynthetic traits and the interaction of multiple small-effect genes pose significant hurdles. Additionally, the acclimation of the photosynthetic machinery to fluctuating environments needs to be better understood to identify relevant genetic variations (Bezouw et al., 2019). Future research should focus on optimizing gene editing and transformation systems, exploring novel genetic resources, and integrating big data approaches to streamline the phenotype-to-gene identification pipeline. Addressing these challenges will pave the way for the development of maize varieties with superior photosynthetic efficiency and yield potential (Agarwal et al., 2018; Wang et al., 2022).

5 Impact of Environmental Factors on Photosynthetic Machinery

5.1 Effects of temperature, light intensity, and CO₂ levels

Environmental factors such as temperature, light intensity, and CO₂ levels significantly influence the photosynthetic machinery of maize. Elevated temperatures can enhance photosynthesis up to an optimal point, beyond which the efficiency declines. For instance, leaf photosynthesis in maize was found to increase with temperature up to 31/25 °C but declined at 37/31 °C, although elevated CO₂ levels could mitigate some of the negative effects of high temperatures by enhancing photosynthesis and reducing transpiration rates (Liu et al., 2022). Additionally, maize's response to light intensity is crucial, as high light can exacerbate latent manganese deficiencies, leading to reduced photosynthetic efficiency (Long et al., 2020). The interplay between CO₂ levels and temperature also plays a critical role, with elevated CO₂ enhancing photosynthesis under high temperatures by increasing leaf soluble sugars and altering stomatal traits (Liu et al., 2022).

5.2 Photosynthetic responses to water availability

Water availability is another critical factor affecting maize photosynthesis. Drought conditions can significantly impair the photosynthetic apparatus, as evidenced by reduced photochemical quenching, electron transport rates, and overall photosynthetic efficiency (Stefanov et al., 2023). Maize exhibits better drought tolerance compared to other crops like sorghum, partly due to its ability to regulate energy losses and activate state transitions under water stress (Stefanov et al., 2023). Moreover, maize genotypes with different drought and heat tolerance levels show varied responses, with some genotypes maintaining photosynthetic rates through increased stomatal conductance or limited transpiration, which acts as a drought avoidance mechanism (Correia et al., 2021).

5.3 Interaction between photosynthesis and nutrient uptake

Nutrient availability, particularly manganese, plays a vital role in the functionality of the photosynthetic apparatus. High light intensity can aggravate latent manganese deficiencies, leading to a decline in photosynthetic performance (Long et al., 2020). Additionally, intercropping maize with wheat can lower nutrient uptake due to competition, although it surprisingly increases the photosynthetic rate of maize's ear leaf, suggesting complex interactions between nutrient availability and photosynthetic efficiency (Gou et al., 2018). These findings highlight the importance of balanced nutrient management to optimize photosynthetic performance in maize.

5.4 Adaptive mechanisms in maize to environmental stressors

Maize has developed several adaptive mechanisms to cope with environmental stressors. For instance, under high temperature and drought conditions, maize can regulate its photosynthetic traits, such as the C₄-CO₂ concentrating mechanism, to maintain efficiency (Correia et al., 2021). The dynamic response of maize to diurnal changes in light and temperature involves significant alterations in protein abundance and phosphorylation, which are crucial for maintaining high photosynthetic capacity (Gao et al., 2022). Additionally, maize's ability to adjust its photosynthetic machinery in response to fluctuating light environments, such as by optimizing the duration of high light exposure, is essential for maximizing photosynthetic productivity and yield (Wu et al., 2022). These adaptive mechanisms underscore the resilience of maize to varying environmental conditions and provide insights for breeding programs aimed at enhancing stress tolerance.

By understanding these complex interactions and adaptive responses, researchers can develop strategies to improve maize's resilience to environmental stressors, ultimately enhancing crop productivity and sustainability.

6 Case Study

6.1 Case study overview

This case study focuses on the molecular insights into the photosynthetic machinery of maize (Zea mays L.) under various environmental conditions. By examining specific genetic and biochemical pathways, this study aim to understand how maize adapts its photosynthetic processes to optimize efficiency and productivity. The study integrates findings from multiple research efforts to provide a comprehensive view of the molecular mechanisms involved.

6.2 Impact of specific environmental conditions on photosynthetic machinery

Environmental conditions such as light intensity, CO2 concentration, and intercropping systems significantly impact the photosynthetic machinery of maize. For instance, maize plants grown under different light intensities exhibit distinct adjustments in their photosynthetic apparatus, particularly in the mesophyll (M) and bundle sheath (BS) chloroplasts. These adjustments include changes in the organization and function of thylakoid complexes, which are crucial for optimizing light absorption and distribution between photosystems (Rogowski et al., 2019). Maize carbonic anhydrase mutants show altered photosynthetic responses under low CO₂ conditions, highlighting the importance of CA in CO₂ signaling and stomatal regulation (Figure 3) (Kolbe et al., 2019). Intercropping systems, such as maize-peanut intercropping, enhance photosynthetic efficiency by improving carbon fixation and carboxylation rates, demonstrating the benefits of sustainable agricultural practices (Ma et al., 2023).

Figure 3 Gene expression patterns in the CO2 signaling pathway of maize stomata (Adapted from Kolbe et al., 2019) Image caption: The expression patterns of genes involved in the CO2 signaling pathway within maize stomatal guard cells. Data for wild-type plants are presented as an average of both wild-type genotypes, shown as log-transformed counts-per-million with standard error bars. The green area represents a maize guard cell, where the bicarbonate (HCO3-) pool generated by carbonic anhydrase-mediated CO2 hydration is detected by RHC1. Elevated bicarbonate levels lead RHC1 to bind HT1, preventing HT1 from inhibiting OST1 (as indicated by the dashed line). With HT1 sequestered at the plasma membrane, OST1 can activate SLAC1, resulting in stomatal closure. Both RHC1 and SLAC1 are expected to localize to the plasma membrane, as depicted (Adapted from Kolbe et al., 2019)

Kolbe et al. (2019) provides a visual representation of the CO₂ signaling pathway within maize stomatal guard cells, focusing on the interactions between key proteins and their role in stomatal closure. The pathway begins with the sensing of bicarbonate, produced from CO₂ by carbonic anhydrase (CA), by the protein RHC1. When bicarbonate levels are high, RHC1 binds to HT1, preventing HT1 from inhibiting OST1. This inhibition allows OST1 to activate SLAC1, leading to the closure of stomata. The figure also includes gene expression data for wild-type and mutant maize plants under varying CO₂ conditions, illustrating how specific genes involved in this pathway are differentially expressed, which highlights the potential conservation of CO₂ signaling mechanisms between species.

6.3 Molecular analysis of photosynthetic efficiency in the case study

Molecular analyses reveal several key factors contributing to photosynthetic efficiency in maize. The carbonic anhydrase gene ZmCA4 plays a critical role in modulating CO₂ signaling and enhancing photosynthetic capacity. Overexpression of ZmCA4 increases rubisco activity, quantum yield, and electron transport rates in photosystem II, leading to improved maize yield-related traits (Zhou et al., 2023). Similarly, the NADH dehydrogenase-like (NDH) complex optimizes carbon flow and redox balance in BS cells, coordinating photosynthetic transcript abundance and protein content (Zhang et al., 2023). Furthermore, integrative analyses of transcriptome, proteome, and phosphoproteome data indicate that brassinosteroid signaling upregulates photosynthesis-related genes and proteins, thereby promoting photosynthetic efficiency (Li et al., 2023b).

6.4 Lessons learned and implications for broader applications

The findings from this case study provide valuable insights into the genetic and molecular mechanisms underlying photosynthetic efficiency in maize. Understanding these mechanisms can inform breeding programs aimed at developing high-yielding and stress-tolerant maize varieties. For example, manipulating genes involved in CO₂ signaling, such as ZmCA4, or optimizing the function of the NDH complex could enhance photosynthetic performance under varying environmental conditions (Zhang et al., 2023; Zhou et al., 2023). Additionally, sustainable agricultural practices like intercropping can be leveraged to improve resource utilization and crop productivity (Ma et al., 2023). These lessons underscore the potential for integrating molecular biology with agronomic practices to achieve food security and sustainable agriculture.

7 Applications of Molecular Insights into Photosynthetic Machinery

7.1 Improving crop yields through enhanced photosynthesis

Molecular insights into the photosynthetic machinery of maize have shown significant potential in improving crop yields. For instance, the constitutive expression of maize GOLDEN2-LIKE (GLK) genes in rice has led to enhanced levels of chlorophylls and pigment-protein antenna complexes, resulting in improved light harvesting efficiency and increased carbohydrate levels. This has translated into a 30~40% increase in both vegetative biomass and grain yield (Li et al., 2020b). Similarly, the insertion of the cyanobacterial membrane protein ictB into maize has increased leaf starch and sucrose content, leading to an average grain yield improvement of 3.49% in field trials (Koester et al., 2021). These findings underscore the potential of genetic modifications to enhance photosynthetic efficiency and, consequently, crop yields.

7.2 Contributions to sustainable agriculture practices

Enhanced photosynthetic efficiency not only boosts crop yields but also contributes to sustainable agriculture practices. For example, the development of climate-smart crops with enhanced photosynthesis can provide novel solutions to increase crop productivity while reducing atmospheric carbon and nitrogen emissions (Jansson et al., 2018). Additionally, the coupling of nitrogen fertilization with iron foliar application has been shown to improve photosynthetic characteristics and nitrogen use efficiency in maize, leading to better growth and higher yields under intercropping systems (Nasar et al., 2022). These practices promote sustainable agriculture by optimizing resource use and minimizing environmental impact.

7.3 Potential for climate resilience in maize cultivars

Molecular insights into photosynthetic machinery also hold promise for developing climate-resilient maize cultivars. Efficient regulation of CO₂ assimilation has been shown to enable greater resilience to high temperature and drought in maize. For instance, maize genotypes with contrasting levels of drought and heat tolerance have demonstrated different mechanisms for maintaining photosynthetic rates under stress conditions, such as increased stomatal conductance and limited transpiration (Correia et al., 2021). These traits can be exploited in breeding programs to develop maize cultivars that are better adapted to the challenges posed by climate change.

7.4 Commercial applications and agronomic benefits

The commercial applications and agronomic benefits of enhanced photosynthetic machinery in maize are substantial. For instance, the use of nontoxic orange carbon dots (o-CDs) has been shown to increase photosynthetic parameters and pigment content in maize, leading to improved photosynthetic efficiency (Milenković et al., 2021). Additionally, the integration of molecular insights into breeding programs has resulted in high-yielding maize hybrids with longer photosynthetic duration and higher chlorophyll content (Yan et al., 2021). These advancements not only improve crop productivity but also offer significant commercial benefits by increasing the profitability and sustainability of maize cultivation.

In summary, molecular insights into the photosynthetic machinery of maize have far-reaching applications in improving crop yields, promoting sustainable agriculture, enhancing climate resilience, and providing commercial and agronomic benefits. These advancements underscore the importance of continued research and innovation in this field to address the growing demands for food and energy in a changing climate.

8 Future Perspectives

8.1 Emerging research areas in photosynthesis in maize

Recent studies have highlighted several emerging research areas in the field of photosynthesis in maize. One promising area is the investigation of the photosynthetic mechanisms under fluctuating light environments. Research has shown that the duration of daily high light exposure significantly impacts photosynthetic rates and biomass yield in maize, suggesting that optimizing light conditions could enhance crop productivity (Wu et al., 2022). Additionally, the role of specific genes, such as ZmCA4, in modulating photosynthetic efficiency and CO₂ signaling pathways has been identified, providing new genetic targets for improving maize yield (Zhou et al., 2023). Another emerging area is the use of hybrid lines, such as oat × maize chromosome addition lines, to understand the functioning of the photosynthetic apparatus under stress conditions, which could lead to the development of more resilient crop varieties (Juzoń et al., 2020).

8.2 Technological advancements and their potential impact

Technological advancements have significantly contributed to our understanding of photosynthesis in maize. High-throughput phenotyping techniques have enabled the monitoring of crop photosynthetic responses to changing environmental conditions, facilitating the development of models to predict plant growth under specific constraints (Baslam et al., 2020). The integration of omics technologies, such as genomics, proteomics, and metabolomics, has provided deeper insights into the genetic and metabolic pathways involved in photosynthesis and stress responses (Li et al., 2020). Additionally, the use of engineered nanoparticles, such as Fe-based nanomaterials, has shown potential in enhancing photosynthetic rates and biomass production, indicating a promising avenue for nano-enabled agriculture (Baslam et al., 2020; Li et al., 2020).

8.3 Integrating omics approaches for a holistic understanding

The integration of omics approaches is crucial for a holistic understanding of photosynthesis in maize. Genomic studies have identified key regulatory genes and pathways that influence photosynthetic efficiency and stress tolerance (Muhammad et al., 2021; Zhou et al., 2023). Proteomic analyses have revealed the impact of environmental factors on the expression of photosynthetic proteins, providing insights into the mechanisms of acclimation and adaptation (Wu et al., 2022). Metabolomic studies have shown how metabolic reprogramming in response to nanoparticle exposure can enhance photosynthesis and plant growth (Li et al., 2020). By combining these omics approaches, researchers can develop comprehensive models that predict how maize plants respond to various environmental conditions, ultimately leading to the development of more efficient and resilient crop varieties.

8.4 Policy and funding considerations for future research

To advance research in photosynthesis in maize, it is essential to consider policy and funding strategies that support long-term and interdisciplinary studies. Funding agencies should prioritize research that integrates advanced technologies and omics approaches to address the complex challenges of improving photosynthetic efficiency and crop yield under changing environmental conditions (Jansson et al., 2018; Baslam et al., 2020). Policies should also encourage collaboration between academic institutions, industry, and government agencies to facilitate the translation of research findings into practical applications. Additionally, investment in training programs for young scientists and the development of research infrastructure will be crucial for sustaining progress in this field. By aligning policy and funding priorities with the emerging research areas and technological advancements, we can accelerate the development of climate-smart crops with enhanced photosynthetic efficiency and resilience (Jansson et al., 2018; Muhammad et al., 2021).

9 Concluding Remarks

The research on the photosynthetic machinery of maize has yielded several significant insights. The role of carbonic anhydrase (CA), particularly ZmCA4, has been highlighted as crucial for photosynthetic efficiency and CO₂ signaling, with its interaction with aquaporin ZmPIP2;6 being essential for optimal photosynthetic performance and yield improvement. The NADH dehydrogenase-like (NDH) complex has been shown to optimize C₄ photosynthetic carbon flow and cellular redox states, directly influencing the carbon flow in maize's two-celled C₄ system. Additionally, the temporal regulation of the metabolome and proteome in maize hybrids has been linked to enhanced photosynthetic efficiency and plant growth, providing insights into the molecular basis of heterosis. Intercropping systems, such as maize-peanut intercropping, have been found to improve photosynthetic characteristics and resource utilization efficiency. Furthermore, the response of maize to low CO₂ conditions has underscored the importance of CA in maintaining photosynthetic efficiency and stomatal signaling. Studies on the acclimation of maize to different light intensities and the role of brassinosteroids in photosynthetic response have also provided valuable information on the regulation and optimization of photosynthesis under varying environmental conditions.

The findings from these studies have significant implications for maize breeding and agricultural practices. The identification of key genes and proteins, such as ZmCA4 and NDH complex components, that enhance photosynthetic efficiency can be targeted in breeding programs to develop high-yielding maize varieties. The understanding of heterosis at the metabolic and proteomic levels can aid in the selection of hybrid combinations that maximize photosynthetic efficiency and growth. The benefits of intercropping systems, particularly maize-peanut intercropping, suggest that adopting such practices can improve resource utilization and crop productivity. Additionally, the insights into the response of maize to low CO₂ and varying light conditions can inform strategies to enhance resilience and performance under suboptimal environmental conditions. The role of brassinosteroids in promoting photosynthesis further opens avenues for the use of plant growth regulators to boost crop productivity.

The future of photosynthesis research in maize holds great promise for advancing our understanding and improving crop performance. Continued integrative studies combining physiological, transcriptomic, proteomic, and metabolomic approaches will be essential to unravel the complex regulatory networks governing photosynthesis. The exploration of genetic variation and the identification of novel molecular targets, such as those involved in non-photochemical quenching and photosystem II efficiency, will be crucial for developing maize varieties with enhanced photosynthetic efficiency and stress tolerance. Moreover, the application of advanced breeding techniques, including gene editing and marker-assisted selection, will enable the precise manipulation of key photosynthetic genes to achieve desired traits. As global challenges such as climate change and food security intensify, the insights gained from photosynthesis research will be instrumental in ensuring sustainable and resilient agricultural systems.

Acknowledgments

Authors sincerely thank all the experts and scholars who reviewed the manuscript of this study. Their valuable comments and suggestions have contributed to the improvement of this study.

Conflict of Interest Disclosure

Authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

Reference

Agarwal A., Yadava P., Kumar K., Singh I., Kaul T., Pattanayak A., and Agrawal P., 2018, Insights into maize genome editing via CRISPR/Cas9, Physiology and Molecular Biology of Plants, 24,: 175-183.

https://doi.org/10.1007/s12298-017-0502-3

Bag P., 2021, Light harvesting in fluctuating environments: evolution and function of antenna proteins across photosynthetic lineage, Plants, 10: 84.

https://doi.org/10.3390/plants10061184

Baslam M., Mitsui T., Hodges M., Priesack E., Herritt M., Aranjuelo Í., and Sanz‐Saez A., 2020, Photosynthesis in a changing global climate: scaling up and scaling down in crops, Frontiers in Plant Science, 11: 20.

https://doi.org/10.3389/fpls.2020.00882

Bezouw R., Keurentjes J., Harbinson J., and Aarts M., 2019, Converging phenomics and genomics to study natural variation in plant photosynthetic efficiency, The Plant Journal, 97: 112-133.

https://doi.org/10.1111/tpj.14190

Borba A., Reyna-Llorens I., Dickinson P., Steed G., Gouveia P., Górska A., Gomes C., Kromdijk J., Webb A., Saibo N., and Hibberd J., 2023, Compartmentation of photosynthesis gene expression in C₄ maize depends on time of day, Plant Physiology, 193: 2306-2320.

https://doi.org/10.1093/plphys/kiad447

Borba A., Serra T., Górska A., Gouveia P., Cordeiro A., Reyna-Llorens I., Kneřová J., Barros P., Abreu I., Oliveira M., Hibberd J., and Saibo N., 2018, Synergistic binding of bHLH transcription factors to the promoter of the maize NADP-ME gene used in C4 photosynthesis is based on an ancient code found in the ancestral C3 state, Molecular Biology and Evolution, 35: 1690-1705.

https://doi.org/10.1093/molbev/msy060

Chen Y., Zhou B., Li J., Tang H., Tang J., and Yang Z., 2018, Formation and change of chloroplast-located plant metabolites in response to light conditions, International Journal of Molecular Sciences, 19: 54.

https://doi.org/10.3390/ijms19030654

Correia P., Silva A., Vaz M., Carmo‐Silva E., and Silva J., 2021, Efficient regulation of CO2 assimilation enables greater resilience to high temperature and drought in maize, Frontiers in Plant Science, 12: 6.

https://doi.org/10.3389/fpls.2021.675546

Crepin A., Kučerová Z., Kosta A., Durand E., and Caffarri S., 2019, Isolation and characterization of a large photosystem i-light harvesting complex ii supercomplex with an additional lhca1-a4 dimer in arabidopsis, The Plant journal : for Cell and Molecular Biology, 6: 7.

https://doi.org/10.1111/tpj.14634

Dai X., Tu X., Du B., Dong P., Sun S., Wang X., Sun J., Li G., Lu T., Zhong S., and Li P., 2021, Chromatin and regulatory differentiation between bundle sheath and mesophyll cells in maize, The Plant Journal: for Cell and Molecular Biology, 8: 7.

https://doi.org/10.1111/tpj.15586

Gao Z., Yang X., Mei Y., Zhang J., Chao Q., and Wang B., 2022, A dynamic phosphoproteomic analysis provides insight into the C4 plant maize (Zea mays L.) response to natural diurnal changes, The Plant Journal: for Cell and Molecular Biology, 3: 10.

https://doi.org/10.1111/tpj.16047

Gou F., Ittersum M., Couëdel A., Zhang Y., Wang Y., Putten P., Zhang L., and Werf W., 2018. Intercropping with wheat lowers nutrient uptake and biomass accumulation of maize, but increases photosynthetic rate of the ear leaf, AoB Plants, 10: 78.

https://doi.org/10.1093/aobpla/ply010

Halpape W., Wulf D., Verwaaijen B., Stasche A., Weber A., Delker C., Eisenhut M., and Bräutigam A., 2023, Transcription factors mediating regulation of photosynthesis, bioRxiv, 6: 76.

https://doi.org/10.1101/2023.01.06.522973

Jang S., and Mennucci B., 2018, Delocalized excitons in natural light-harvesting complexes, Reviews of Modern Physics, 11: 12.

https://doi.org/10.1103/RevModPhys.90.035003

Jansson C., Vogel J., Hazen S., Brutnell T., and Mockler T., 2018, Climate-smart crops with enhanced photosynthesis, Journal of Experimental Botany, 69: 3801-3809.

https://doi.org/10.1093/jxb/ery213

Juzoń K., Idziak-Helmcke D., Czyczyło-Mysza I., Dziurka K., and Skrzypek E., 2020., Functioning of the photosynthetic apparatus in response to drought stress in oat maize addition lines, International Journal of Molecular Sciences, 21: 90-100.

https://doi.org/10.3390/ijms21186958

Koester R., Pignon C., Kesler D., Willison R., Kang M., Shen Y., Priest H., Begemann M., Cook K., Bannon G., and Oufattole M., 2021, Transgenic insertion of the cyanobacterial membrane protein ictB increases grain yield in Zea mays through increased photosynthesis and carbohydrate production, PLoS ONE, 16: 35-40.

https://doi.org/10.1371/journal.pone.0246359

Kolbe A., Studer A., Cornejo O., and Cousins A., 2019. Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO_2, BMC Genomics, 20: 56-67.

https://doi.org/10.1186/s12864-019-5522-7

Li H., He X., Gao Y., Liu W., Song J., and Zhang J., 2023b, Integrative analysis of Transcriptome, Proteome, and Phosphoproteome reveals potential roles of photosynthesis antenna proteins in response to brassinosteroids signaling in maize, Plants, 12: 89-90.

https://doi.org/10.3390/plants12061290

Li P., Wang A., Du W., Mao L., Wei Z., Wang S., Yuan H., Ji R., and Zhao L., 2020a, Insight into the interaction between fe-based nanomaterials and maize (Zea mays) plants at metabolic level, The Science of the Total Environment, 738: 139795.

https://doi.org/10.1016/j.scitotenv.2020.139795

Li R., He Y., Chen J., Zheng S., and Zhuang C., 2023a, Research progress in improving photosynthetic efficiency, International Journal of Molecular Sciences, 24: 87.

https://doi.org/10.3390/ijms24119286

Li X., Wang P., Li J., Wei S., Yan Y., Yang J., Zhao M., Langdale J., and Zhou W., 2020b, Maize golden2-like genes enhance biomass and grain yields in rice by improving photosynthesis and reducing photoinhibition, Communications Biology, 3: 87.

https://doi.org/10.1038/s42003-020-0887-3

Lima-Melo Y., Kılıç M., Aro E., and Gollan P., 2021, Photosystem I inhibition, protection and signalling: knowns and unknowns, Frontiers in Plant Science, 12: 124.

https://doi.org/10.3389/fpls.2021.791124

Liu H., Jian L., Xu J., Zhang Q., and Yan J., 2020, High-Throughput CRISPR/Cas9 mutagenesis streamlines trait gene identification in maize, Plant Cell, 32: 1397-1413.

https://doi.org/10.1105/tpc.19.00934

Liu J., Lu Y., Hua W., and Last R., 2019, A new light on photosystem maintenance in oxygenic photosynthesis, Frontiers in Plant Science, 10: 75.

https://doi.org/10.3389/fpls.2019.00975

Liu L., Gallagher J., Arevalo E., Chen R., and Jackson D., 2021, Enhancing grain-yield-related traits by CRISPR–Cas9 promoter editing of maize CLE genes, Nature Plants, 7: 287-294.

https://doi.org/10.1038/s41477-021-00858-5

Liu L., Hao L., Zhang Y., Zhou H., Ma B., Cheng Y., Tian Y., Chang Z., and Zheng Y., 2022, The CO₂ fertilization effect on leaf photosynthesis of maize (Zea mays L.) depends on growth temperatures with changes in leaf anatomy and soluble sugars, Frontiers in Plant Science, 13: 78.

https://doi.org/10.3389/fpls.2022.890928

Lokstein H., Renger G., and Götze J., 2021, Photosynthetic light-harvesting (antenna) complexes-structures and functions, Molecules, 26: 178.

https://doi.org/10.3390/molecules26113378

Long L., Pedas P., Kristensen R., Schulze W., Husted S., Zhang G., Schjoerring J., and Yuan L., 2020, Latent mn deficiency in maize is aggravated by high light intensity as revealed by physiological, transcriptomic and proteomic analyses, Journal of Experimental Botany, 3: 366-387.

https://doi.org/10.1093/jxb/eraa366

Lorenzo C., Debray K., Herwegh D., Develtere W., Impens L., Schaumont D., Vandeputte W., Aesaert S., Coussens G., Boe Y., Demuynck K., Hautegem T., Pauwels L., Jacobs T., Ruttink T., Nelissen H., and Inzé D., 2022, Breedit: a multiplex genome editing strategy to improve complex quantitative traits in maize, The Plant Cell, 4: 243.

https://doi.org/10.1093/plcell/koac243

Ma C., Feng Y., Wang J., Zheng B., Wang X., and Jiao N., 2023, Integrative physiological, transcriptome, and proteome analyses provide insights into the photosynthetic changes in maize in a maize-peanut intercropping system, Plants, 1: 86.

https://doi.org/10.3390/plants13010065

Milenković I., Borišev M., Zhou Y., Spasic S., Leblanc R., and Radotić K., 2021, Photosynthesis enhancement in maize via nontoxic orange carbon dots, Journal of Agricultural and Food Chemistry, 298: 87-89.

https://doi.org/10.1021/acs.jafc.1c01094

Muhammad I., Shalmani A., Ali M., Yang Q., Ahmad H., and Li F., 2021, Mechanisms regulating the dynamics of photosynthesis under abiotic stresses, Frontiers in Plant Science, 11: 43-78.

https://doi.org/10.3389/fpls.2020.615942

Nasar J., Wang G., Ahmad S., Muhammad I., Zeeshan M., Gitari H., Adnan M., Fahad S., Khalid M., Zhou X., Abdelsalam N., Ahmed G., and Hasan M., 2022, Nitrogen fertilization coupled with iron foliar application improves the photosynthetic characteristics, photosynthetic nitrogen use efficiency, and the related enzymes of maize crops under different planting patterns, Frontiers in Plant Science, 13: 66-89.

https://doi.org/10.3389/fpls.2022.988055

Pan X., Ma J., Su X., Cao P., Chang W., Liu Z., Zhang X., and Li M., 2018, Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II, Science, 360: 1109-1113.

https://doi.org/10.1126/science.aat1156

Rogowski P., Wasilewska-Dębowska W., and Romanowska E., 2019, Photosynthesis and organization of maize mesophy and bundle sheath thylakoids of plants grown in various light intensities, Environmental and Experimental Botany, 19: 6.

https://doi.org/10.1016/J.ENVEXPBOT.2019.02.006

Sharwood R., Quick W., Sargent D., Estavillo G., Silva-Pérez V., and Furbank R., 2022, Mining for allelic gold: finding genetic variation in photosynthetic traits in crops and wild relatives, Journal of Experimental Botany, 81: 7654-7659.

https://doi.org/10.1093/jxb/erac081

Stefanov M., Rashkov G., Borisova P., and Apostolova E., 2023, Sensitivity of the photosynthetic apparatus in maize and sorghum under different drought levels, Plants, 12: 64.

https://doi.org/10.3390/plants12091863

Steinbeck J., Ross I., Rothnagel R.,Takahashi Y., Hippler M., and Hankamer B., 2018, Structure of a PSI–LHCI–cyt b6f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions, Proceedings of the National Academy of Sciences, 115: 10517-10522.

https://doi.org/10.1073/pnas.1809973115

Stirbet A., Lazár D., Guo Y., and Govindjee G., 2019, Photosynthesis: basics, history, and modeling, Annals of Botany, 3: 171.

https://doi.org/10.1093/aob/mcz171

Tao S., Liu P., Shi Y., Feng Y., Gao J., Chen L., Zhang A., Cheng X., Wei H., Tao Z., and Zhang W., 2022, Single-cell transcriptome and network analyses unveil key transcription factors regulating mesophyll cell development in maize, Genes, 13: 90.

https://doi.org/10.3390/genes13020374

Vayghan H., Nawrocki W., Schiphorst C., Tolleter D., Hu C., Douet V., Glauser G., Giovanni F., Croce R., Wientjes E., and Longoni F., 2021, Photosynthetic light harvesting and thylakoid organization in a CRISPR/Cas9 Arabidopsis Thaliana LHCB1 knockout mutant, Frontiers in Plant Science, 13: 34.

Wang B., Zhu L., Zhao B., Zhao Y., Xie Y., Zheng Z., Li Y., Sun J., and Wang H., 2019, Development of a haploid-inducer mediated genome editing system for accelerating maize breeding, Molecular Plant, 12(4): 597-602.

https://doi.org/10.1016/j.molp.2019.03.006

Wang J., Yu L., Wang W., Yan Q., Kuang T., Qin X., and Shen J., 2021, Structure of plant photosystem I-light harvesting complex I supercomplex at 2.4 resolution, Journal of Integrative Plant Biology, 78: 90.

https://doi.org/10.1111/jipb.13095

Wang Y., Tang Q., Pu L., Zhang H., and Li X., 2022, CRISPR-cas technology opens a new era for the creation of novel maize germplasms, Frontiers in Plant Science, 13: 87-90.

https://doi.org/10.3389/fpls.2022.1049803

Wu H., Qiao M., Zhang Y., Kang W., Ma Q., Gao H., Zhang W., and Jiang C., 2022, Photosynthetic mechanism of maize yield under fluctuating light environments in the field, Plant physiology, 5: 76.

https://doi.org/10.1093/plphys/kiac542

Yan Y., Hou P., Duan F., Niu L., Dai T., Wang K., Zhao M., Li S., and Zhou W., 2021, Improving photosynthesis to increase grain yield potential: an analysis of maize hybrids released in different years in China, Photosynthesis Research, 150: 295-311.

https://doi.org/10.1007/s11120-021-00847-x

Yi Q., López-Malvar A., Álvarez-Iglesias L., Romay M., and Revilla P., 2023, Genome-wide association analysis identified newly natural variation for photosynthesis-related traits in a large maize panel, Agronomy, 13: 4.

https://doi.org/10.3390/agronomy13030801

Zhang Q., Tian S., Chen G., Tang Q., Zhang Y., Fleming A., Zhu X., and Wang P., 2023, Regulatory NADH dehydrogenase-like complex optimizes C4 photosynthetic carbon flow and cellular redox in maize, The New Phytologist, 4: 5.

https://doi.org/10.1111/nph.19332

Zhao X., Niu Y., Hossain Z., Zhao B., Bai X., and Mao T., 2023, New insights into light spectral quality inhibits the plasticity elongation of maize mesocotyl and coleoptile during seed germination, Frontiers in Plant Science, 14: 9.

https://doi.org/10.3389/fpls.2023.1152399

Zhou J., and Xu L.M., 2024, Conventional breeding vs. genetic engineering in maize: a comparative study, Maize Genomics and Genetics, 15(2): 49-59.

Zhou L., Xiang X., Ji D., Wang J., and Liu C., 2023, A carbonic anhydrase, ZmCA4, contributes to photosynthetic efficiency, and modulates CO₂ signaling gene expression by interacting with aquaporin ZmPIP2;6 in maize, Plant & Cell Physiology, 11: 8.

https://doi.org/10.1093/pcp/pcad145