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Review

C2 Resilient Photosynthesis: A Practical Option for Long-Term Stable Carbon Sinks?

by
Junjie Zhu
* and
Fengyue Chen
Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning 530004, China
*
Author to whom correspondence should be addressed.
Biology 2026, 15(1), 5; https://doi.org/10.3390/biology15010005
Submission received: 20 November 2025 / Revised: 11 December 2025 / Accepted: 18 December 2025 / Published: 19 December 2025
(This article belongs to the Section Plant Science)
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Simple Summary

C2 photosynthesis enhances net CO2 assimilation by capturing, concentrating, and reassimilating CO2 released during photorespiration, all while minimizing the additional energy expenditure. This process significantly improves carbon uptake, particularly under stress conditions. This review provides an overview of the diversity, distribution, evolution, and environmental resilience of C2 plants, highlighting their potential to stabilize carbon assimilation in the face of climate variability. It also addresses critical research gaps, including the identification of additional C2 species and the need for a deeper understanding of their molecular and ecological mechanisms. The review advocates for a more focused research effort to fully exploit the potential of C2 photosynthesis in enhancing climate resilience.

Abstract

In recent years, extreme climate events such as high temperatures and droughts have become increasingly frequent and intense, posing significant threats to the carbon sink stability of C3, C4, and CAM plants. As a result, identifying photosynthetic strategies that balance adaptability with resilience has emerged as a critical focus in carbon sink research. C2 photosynthesis offers a promising solution by recycling photorespiratory CO2 through the glycine shuttle between mesophyll cells (MCs) and bundle sheath cells (BSCs), thereby optimizing carbon concentration and recovery without additional ATP expenditure, thus minimizing carbon loss. This review provides a comprehensive analysis of the diversity, distribution, evolutionary status, and regulatory mechanisms of C2 photosynthesis, emphasizing its physiological and ecological resilience in carbon sequestration. In comparison to C3 and C4 pathways, C2 photosynthesis demonstrates distinct carbon sink resilience, positioning it as a vital strategy for addressing both current and future global climate challenges. The review also highlights existing gaps in C2 research, particularly in species identification, molecular mechanisms, and ecological studies, and recommends prioritizing these areas to fully harness its potential for enhancing climate resilience.

1. Introduction

The carbon sink function refers to the process by which ecosystems capture atmospheric CO2 and convert it into organic carbon through photosynthesis, thereby storing it long-term [1]. As the primary metabolic pathway for carbon fixation, plant photosynthetic pathways directly influence the rate, magnitude, and stability of carbon sequestration by regulating key enzyme activities, optimizing CO2 supply efficiency, and minimizing photorespiratory losses [2]. However, global climate change is significantly altering the carbon absorption patterns of terrestrial ecosystems, imposing complex impacts on the carbon sequestration capacity of plants with different photosynthetic pathways. In this context, climate projections indicate that future growing seasons will generally be hotter and drier, characterized by more uneven precipitation and increased climate variability. This issue is especially pressing in tropical regions, where extreme weather events—such as droughts followed by floods—frequently disrupt plant growth, severely undermining carbon sequestration capacity. Furthermore, atmospheric CO2 concentrations are expected to exceed 500 μmol/mol by 2050, which will impact plants with different photosynthetic pathways in varying ways [1].
For C3 plants, high-CO2 environments confer theoretical advantages: elevated CO2 concentrations increase Rubisco’s affinity for CO2, reduce photorespiration, and enhance overall carbon fixation, providing growth advantages under normal climatic conditions [3]. However, these benefits are largely negated under high-temperature and drought stress. High temperatures increase Rubisco’s oxygenase activity, reinstating photorespiratory activity, while drought stress induces stomatal closure, thereby reducing CO2 availability to the plant. These combined factors exacerbate photorespiration, and elevated CO2 concentrations can perturb the carbon-to-nitrogen (C/N) ratio and trigger source-sink imbalances, further reducing the carbon sequestration efficiency of C3 plants [4]. In contrast, C4 plants intrinsically mitigate photorespiratory losses through their unique CO2 concentration mechanism, augmenting photosynthetic efficiency and water use efficiency (WUE) under high-temperature and high-irradiance conditions. However, in cooler regions with abundant rainfall, their photosynthetic carbon sequestration capacity is significantly constrained, limiting their potential [5]. While CAM plants can maintain a degree of carbon sink functionality in arid environments by fixing CO2 at night and minimizing water loss, their low productivity and narrow distribution make them ill-suited for large-scale carbon sequestration applications [6].
Given the environmental fluctuations induced by global climate change, plants relying on a single photosynthetic pathway face inherent limitations in maintaining stable carbon sinks. Therefore, identifying photosynthetic strategies that can adapt to diverse environmental stresses while sustaining carbon sink functions has become a key focus in carbon sequestration research. Fortunately, a distinctive photosynthetic pathway has garnered growing attention in recent years. In the 1970s, Kennedy and Laetsch first identified the C2 photosynthetic pathway, classifying it as a C3–C4 intermediate [7]. This perspective prevailed for nearly four decades until Sage’s 2012 study demonstrated that C2 photosynthesis represents a transitional strategy in the evolutionary shift from C3 to C4 photosynthesis [8]. C2 plants concentrate CO2 through photorespiratory glycine shuttling: glycine is synthesized in mesophyll cells (MCs), transported to BSCs for decarboxylation, and the released CO2 is re-fixed by Rubisco in the BSCs [9]. This “glycine shuttle” or “photorespiratory CO2 pump” reduces the CO2 compensation point, mitigates photorespiratory carbon losses, and improves carbon assimilation efficiency. Notably, C2 plants exhibit remarkable metabolic plasticity, with the ability to switch between C3 and C3–C4 photosynthetic modes depending on environmental conditions. Some species even exhibit weak C4 traits [10,11,12]. This flexibility mitigates photorespiration during stomatal closure and aids C2 plants in adapting to saline soils, which can exacerbate photorespiration, endowing C2 photosynthesis with distinct adaptive advantages in flood-prone areas associated with soil salinization. Studies have shown that C2 plants not only recover photorespiratory CO2 efficiently but also enhance WUE in low CO2 environments, where photorespiration tends to increase. Their improved adaptability to climate change and tolerance to abiotic stresses [13] position them as promising candidates for resilient carbon sinks in the face of global climate change. As research on C2 plants progresses, significant advances have been made in understanding their species diversity, geographical distribution, phylogenetic relationships, structural characteristics, and physiological and molecular mechanisms. Comparative studies with C3 and C4 plants have elucidated the carbon fixation resilience of C2 plants and their potential as carbon sinks. However, challenges remain, including the complexity of C2 plant identification, an incomplete understanding of their molecular mechanisms compared to C3 and C4 plants, and unresolved issues related to the genetic stability of engineered C2 plants.
This paper provides a systematic review of the diversity, distribution patterns, evolutionary status, and physiological and molecular mechanisms of C2 photosynthesis. By comparing it with C3 and C4 pathways, it further explores C2 photosynthesis’ performance under both normal and stressed conditions, emphasizes its resilience in maintaining global carbon sink stability, and lays the groundwork for future research and development in this area.

2. Diversity, Distribution, and Evolutionary Status of C2 Plants

Sage and Khoshravesh proposed the concept of passive CO2 concentration mechanisms (pCCMs), in which plants do not expend additional ATP but instead “trap” CO2 released during photorespiration or respiration in a localized region around Rubisco [14]. A diffusion barrier between this region and the leaf’s outer airspaces promotes CO2 enrichment in this localized microenvironment. They established four criteria for identifying passive carbon concentration mechanism-dependent carbon concentration mechanisms (CCMDE): No additional ATP or reducing power is consumed. Local CO2 concentrations exceed those achievable through atmospheric diffusion. CO2 enrichment is facilitated by metabolic CO2 release or structural adaptations. A diffusion barrier exists between the high-CO2 region and the leaf’s outer airspaces. Based on these criteria, the C2 photosynthetic pathway is considered one of the most efficient forms of pCCMs in higher plants [14], a view that is widely accepted within the scientific community. Khoshravesh et al. further advanced the identification of C2 plants by developing reliable methods, including the detection of high-activity glycine decarboxylase (GDC) in BSCs, immunohistochemical analyses, ultrastructural observations of leaf tissues, and measurement of CO2 compensation points [15]. However, the practical implementation of these techniques remains laborious, underscoring the need for more efficient and accessible identification protocols in future research. To date, the C2 photosynthetic pathway has been documented in over 70 species across 13 families, including 4 monocot and 9 eudicot groups. Prominent plant families with abundant C2 species include Poaceae, Acanthaceae, Asteraceae, Amaranthaceae, Boraginaceae, Brassicaceae, and Portulacaceae (Table 1). C2 plants display substantial intraspecific and intraindividual photosynthetic diversity and plasticity [11], suggesting that additional C2 species are likely to be discovered in the foreseeable future.
Geographically, C2 plants are distributed across all continents except Antarctica, with greater representation in the Southern and Western Hemispheres. They are particularly abundant in regions such as Australia, the Americas, Western Europe’s Atlantic coast, and South Africa. Furthermore, C2 plants show considerable ecological and geographical diversity, encompassing both widespread and endemic species [47,48].
There are three primary hypotheses concerning the evolutionary status of C2 plants:
  • The Evolutionary “Bridge” Hypothesis: This hypothesis posits that C2 plants function as an evolutionary intermediate, mediating the evolutionary transition from C3 to C4 photosynthesis, thus laying the groundwork for the eventual evolution of C4 plants. Two supporting subtheories are proposed: the Nitrogen Hypothesis, which suggests that reduced photorespiration in C3 plants (through glycine shuttling, which releases ammonium into the bundle sheath cells (BSCs)) perturbs foliar nitrogen metabolism. To restore this balance, C2 photosynthesis would evolve into C4 photosynthesis, which is more nitrogen-use efficient [49,50]. The Environmental Hypothesis argues that C2 photosynthesis enhances carbon assimilation efficiency under high-temperature conditions, thereby enabling plant lineages to colonize warmer habitats than those occupied by their C3 relatives. These environments amplify photorespiratory losses, thereby imposing selective pressure on C2 plants and accelerating their evolutionary transition to C4 photosynthesis [26,51].
  • The Stable Photosynthetic Type Hypothesis: According to this hypothesis, C2 photosynthesis represents a stable photosynthetic strategy that is evolutionarily parallel to C3 and C4 pathways, and does not necessarily evolve into C4 photosynthesis. Supporting evidence includes: (1) anatomical constraints on metabolite exchange and cooler climates that inhibit the further evolution of C2 photosynthesis into C4, (2) the physiological adequacy of C2 photosynthesis for plant survival in certain environments, and (3) the persistence of C2 photosynthesis within specific lineages (e.g., Portulaca species) for millions of years without transitioning to C4 photosynthesis [52]. Furthermore, in Chenopodiaceae, C2-type species exhibit distinct upregulation of transcription factors, further suggesting that C2 represents an evolutionarily stable state within these taxa [15].
  • The Hybrid Origin Hypothesis: This theory proposes that C2 photosynthesis originates from interspecific hybridization events between C3 and C4 lineages. For example, the C2-type Salsola divaricata complex (Amaranthaceae) results from hybridization between C3 and C4 ancestors, enabling the species to adapt to a wider range of climatic conditions [23]. Similar hybrid-origin phenomena have also been observed in species such as Diplotaxis and Homolepis isocalycia [53,54,55].

3. Brief Overview of the Mechanisms of C2 Photosynthesis

C2 photosynthesis functions primarily as a photorespiratory carbon pump, recycling and reutilizing CO2 released during photorespiration through a series of anatomical, physiological, biochemical, and molecular processes.

3.1. Leaf Structural Adaptations in C2 Photosynthesis

Anatomically, C2 plants (both monocots and eudicots) possess Kranz-like leaf anatomical architectures in contrast to C3 plants. Notably, the ratio of BSC area to MC area is increased, and organelles (notably mitochondria and chloroplasts) are more densely packed, often concentrated near the BS cell walls (Figure 1).
This anatomical configuration provides the structural foundation for CO2 concentration: CO2 released during photorespiration accumulates in the BSCs, thereby enhancing Rubisco’s carboxylation efficiency. Furthermore, the density of plasmodesmata at the interface between BSCs and parenchyma cells is increased, facilitating metabolite transport. These anatomical features are integral to the efficient concentration of CO2 within the BSCs—a key component of the C2 photosynthetic pathway [56,57]. For a detailed comparison of leaf traits among C2, C3, and C4 plants, refer to Supplementary Materials Table S1.

3.2. Core Physiological and Biochemical Mechanisms of C2 Photosynthesis

A key characteristic of C2 photosynthesis is the specific localization of glycine decarboxylase within BSCs. In plants that utilize C2 photosynthesis, glycine decarboxylase (GDC) is mainly found in the mitochondria of BSCs, with significantly reduced activity in MCs [58,59]. This enzyme catalyzes the decarboxylation of two glycine molecules, producing one serine molecule while releasing one molecule of carbon dioxide and ammonia. GDC consists of four subunits: the P-protein, which contains a pyridoxal phosphate cofactor; the T-protein, which contains tetrahydrofolate; the H-protein, which contains a lipoamide cofactor; and the L-protein. Among these subunits, the P-protein functions as the key catalytic site. The cell-specific distribution of this enzyme enables the transport of glycine—produced through photorespiration—between MCs and BSCs. Specifically, glycine is synthesized in MCs, then transported to BSCs where decarboxylation occurs. The carbon dioxide released during this process is subsequently re-fixed by the enzyme Rubisco in BSCs. This mechanism reduces carbon loss associated with photorespiration and improves overall carbon assimilation efficiency. Research has shown that the carbon dioxide compensation point of C2 photosynthetic plants typically ranges from 10 to 40 micromoles per mole, which is considerably lower than that of C3 photosynthetic plants but higher than that of C4 photosynthetic plants (less than 10 micromoles per mole). Short-term 14CO2 labeling experiments and model analyses have revealed that in Flaveria pubescens—a plant that employs C2 photosynthesis—the in vivo ratio of carboxylation to oxygenation is more than three times higher than that of C3 photosynthetic plants [60]. This finding provides evidence that the photorespiratory carbon pump effectively increases the concentration of carbon dioxide in BSCs, a critical factor in enhancing the carbon fixation efficiency of C2 photosynthetic plants.

3.3. Key Molecular Mechanisms of C2 Photosynthesis

At the molecular level, the establishment of C2 photosynthesis involves extensive regulation of gene expression and reprogramming of metabolic networks. Several key molecular mechanisms underpin this process, including the re-localization of GDC, transcription factor regulation, and metabolite accumulation. The specific localization of GDC in BSCs is a central molecular event in the evolution of C2 photosynthesis, driven by a fundamental shift in the expression pattern of the GDC subunit GLDP1. In C3 plants, GLDP1 is expressed in both MCs and BSCs, but in C2 plants, it is predominantly expressed in BSCs, with significantly reduced or silenced expression in MCs. This shift is regulated by cis-regulatory elements and transcription factors. Key cis-elements (e.g., M-box) have been identified as mediators of MC expression, and transcription factor binding sites (e.g., MYC and MYB) within the GLDP1 promoter region collectively modulate GLDP1 expression levels [61]. Transposon insertion plays a critical role in reshaping the evolution of C2 photosynthesis. In Arabidopsis thaliana (a C3 plant), regulatory sequences within the GLDP1 promoter ensure its partial expression in MCs. However, in C2 species such as Moricandia arvensis, transposon insertion deactivates the cis-elements (e.g., M-box) responsible for maintaining MC expression, thus restricting GLDP1 expression to BSCs. This shift in expression pattern is essential for the glycine shuttling mechanism central to C2 photosynthesis. Notably, this transposon-mediated reshaping of GDC expression patterns has occurred independently in several distantly related plant lineages, such as Brassicaceae, Asteraceae, and Poaceae, providing an example of convergent evolution at the molecular level [62]. Metabolomic studies have revealed unique metabolic signatures in C2 plants, including distinct patterns of metabolite accumulation (e.g., glycine, serine, and malate), which reflect active carbon and nitrogen shuttling [63]. Additionally, α-ketoglutarate (AKG) has been identified as a critical regulator in the transition from C2 to C4 photosynthesis by modulating nitrogen metabolism and carbon flux, thereby promoting the evolution of the C4 metabolic pathway [64]. Research on the molecular regulatory networks governing C2 photosynthesis is still in its early stages. Only approximately 70 C2 plant species have been identified (Table 1), and significant gaps remain in understanding the molecular mechanisms that govern traits specific to C2 plants, such as leaf anatomical differentiation and gene expression patterns.

4. Physiological Ecology Perspectives on the Resilience of C2 Photosynthesis

Assimilating and fixing carbon dioxide through photosynthesis is an efficient, economical, and sustainable mechanism for regulating global carbon sink capacity. Photosynthesis not only converts atmospheric carbon dioxide into valuable biomolecules (e.g., proteins, lipids, and carbohydrates) but also captures solar energy and converts it into bioenergy, thereby supporting the proper functioning of global energy and carbon cycles.

4.1. Intrinsic Resilience: High-Efficiency Carbon Capture and Energy Conservation

Historically, research on carbon fixation and sequestration has primarily focused on C3 and C4 plants. However, increasing attention is now being directed toward C2 photosynthesis. The carbon fixation pathways of C3, C4, and C2 plants are depicted in Figure 2, highlighting key differences in CO2 absorption, utilization, and photorespiration.
The oval box indicates the enzymes involved in carbon assimilation and photorespiration. Light gray arrows denote areas of low or negligible metabolic activity, while darker green arrows signify regions of heightened carbon assimilation capacity. Darker orange arrows represent areas with increased photorespiratory activity. Yellow boxes correspond to plasmodesmata. Red arrows illustrate the concurrent processes of photorespiration and carbon assimilation, whereas blue arrows depict the distinct amino acid transport mechanisms in C2 plants. Green arrows highlight the carbon assimilation pathways specific to C2 and C4 plants.
(a) C3 photosynthesis: In C3 plants, CO2 enters through the stomata and is fixed by Rubisco in the chloroplasts of both mesophyll and bundle sheath cells (when chloroplasts are present). The byproducts of photorespiration are recycled within the mitochondria via the glycine shuttle, releasing CO2 as a byproduct.
(b) C2 photosynthesis: In C2 plants, bundle sheath cells exhibit an increased size, and the glycine shuttle is specifically localized within the mitochondria of these cells. The products of photorespiration are subsequently transported back to the mesophyll cells, where they are utilized in photosynthesis.
(c) C4 Photosynthesis: In C4 plants, Kranz anatomy is present, facilitating the full C4 cycle. CO2 is initially assimilated in the mesophyll cells and subsequently transferred to the bundle sheath cells, where Rubisco is localized to perform the Calvin–Benson cycle.
(d) CAM Photosynthesis: In CAM plants, CO2 is initially assimilated in the mesophyll cells during the night and subsequently transferred to the bundle sheath cells during the day. Within the bundle sheath cells, Rubisco is localized to facilitate the Calvin–Benson cycle.
Both C2 and C3 plants rely on Rubisco for initial CO2 fixation, which competes with O2 molecules. However, C2 plants exhibit enhanced CO2 assimilation capacity due to the re-fixation of photorespiratory CO2 in the BSCs, enabling efficient CO2 absorption even under low CO2 concentrations [60]. Additionally, some C2 plants display moderate phosphoenolpyruvate carboxylase (PEPC) activity, further facilitating CO2 uptake and utilization [50]. In contrast, C4 photosynthesis fixes CO2 into organic acids via PEPC, which significantly reduces the proportion of CO2 released through stomata, thus offering distinct advantages over both C2 and C3 plants. However, C4 photosynthesis is severely inhibited under low temperatures, diminishing its advantages [65]. Photorespiration, a metabolic pathway that consumes energy and carbon during photosynthesis, varies significantly among different photosynthetic types (refer to Supplementary Materials Table S2 for detailed comparisons of photorespiratory parameters among C2, C3, and C4 plants). In C3 plants, photorespiratory carbon loss can exceed 20% of photosynthetically fixed carbon, with most of the released CO2 not being re-fixed [60]. In contrast, C2 plants optimize photorespiration through a metabolic division of labor between MCs and BSCs, significantly improving the recovery rate of photorespiratory carbon [66]. The markedly lower CO2 compensation point of C2 plants (compared to C3 plants) further attests to the efficiency of their carbon concentration mechanism [60]. For example, in Flaveria species, the CO2 compensation point of C2 species lies between that of C3 and C4 species, but closer to C4 species, reflecting a higher carbon sink efficiency than C3 plants [67]. Both empirical measurements and model simulations indicate that, under normal environmental conditions, C2 plants generally exhibit stronger carbon capture and assimilation capabilities than closely related C3 plants (refer to Supplementary Materials Table S3). While C4 plants rely on the C4 cycle to increase CO2 concentration in BSCs and strongly inhibit photorespiration, this pathway requires additional ATP to drive PEPC-mediated CO2 fixation. In contrast, C2 photosynthesis leverages the energy generated by photorespiration to concentrate CO2, eliminating the need for additional energy input [68]. From an energy efficiency standpoint, C2 photosynthesis is more energy-efficient than the C4 pathway, conferring a competitive advantage in resource-limited environments. It is also worth noting that the carbon-concentrating efficiency of the C2 pathway has a theoretical upper limit, constrained by the rate of photorespiration. By contrast, C4 photosynthesis benefits from a more efficient biochemical pump (PEPC), which concentrates CO2 in BSCs, minimizing photorespiration and enabling a higher carbon gain—up to 50% more than C3 plants under high-temperature and high-light conditions.

4.2. Strong Plasticity in Fluctuating Environments

C2 photosynthesis exhibits remarkable plasticity, enabling adaptation to fluctuating environmental conditions. This plasticity arises from the synergistic interaction of multiple biological levels, as outlined below: Under stress conditions, C2 plants exhibit unique gene expression profiles that distinguish them from C3 and C4 species, enabling rapid environmental adaptation [13,53]. For instance, certain C2 species in families such as Amaranthaceae and Chenopodiaceae upregulate the expression of photosynthetic enzyme genes (e.g., PEPC and NADP-ME) while downregulating specific transporter genes under stress, forming a stress-adapted gene regulatory network that supports biochemical and metabolic adjustments [53]. Building on gene expression regulation, C2 plants can upregulate key enzyme activities in response to different stress types, thereby maintaining photosynthetic metabolism. For example, under high-temperature and drought stress, several C2 plants significantly enhance GDC activity to ensure the proper functioning of the photorespiratory pump. Under salt stress, Sedobassia sedoides increases the activity of core enzymes involved in cyclic electron transport, thereby enhancing cyclic electron flow to supplement ATP production for metabolic processes and improving stress response efficiency [24]. Enzyme activity adjustments optimize metabolic flux distribution and activate synergistic mechanisms across key metabolic pathways. In response to abiotic stresses (e.g., drought and high temperatures), certain C2 plants activate the synergistic interaction between photorespiratory carbon recovery and PEPC-assisted carbon fixation through hierarchical regulation of genes and enzymes. This redundancy minimizes the impact of environmental fluctuations on metabolic processes [50]. Moreover, the redistribution of metabolic flux enhances the utilization of nutrients such as nitrogen and sulfur. These three levels of adjustment enable C2 plants to maintain higher water use efficiency (WUE) and carbon assimilation under drought and high-temperature stress, as well as adapt to salt stress by enhancing C4 traits (e.g., increased PEPC activity) or reducing C2 traits, further demonstrating their flexibility in responding to diverse stresses [69,70,71,72,73]. Empirical experiments confirm the carbon sink resilience of C2 photosynthesis under various stress conditions, including combined stresses (refer to Supplementary Materials Table S4). Model simulations also indicate that introducing the C2 mechanism into C3 crops (e.g., rice) results in a stable ~10% increase in carbon sequestration under most conditions, without the potential losses observed in C4 plants under high-CO2 or low-irradiance environments [18,68]. These findings suggest that C2 photosynthesis can maintain stable carbon sinks in fluctuating environments through synergistic molecular-to-physiological mechanisms, offering unique advantages in mitigating global climate change. However, while C2 plants are widely distributed, they tend to occupy specific ecological niches and, though advantageous in stress-prone environments, often exhibit lower productivity compared to C4 plants in resource-abundant settings.

4.3. Advantage Analysis of C2 Photosynthesis Compared to C4 Photosynthetic Engineering Modifications

Under certain environmental conditions, C4 plants require less nitrogen and water than C3 plants, resulting in higher photosynthetic productivity [74]. This gives C4 plants a stronger carbon sink capacity in grassland and agricultural ecosystems. As global temperatures continue to rise, the advantages of C4 plants over C3 plants in carbon sink function are expected to increase [75]. Considering this, bioengineering efforts have aimed to transform C3 plants into C4-functional plants, as exemplified by projects such as the C4 Rice Project [76] and the C4 transformation of wheat [77]. While these efforts have enhanced photosynthetic carbon assimilation and drought adaptation, they face significant challenges, including structural modifications (e.g., increasing minor vein density and expanding BSC area) and genetic hurdles (e.g., gene silencing, interspecific incompatibility, and multi-gene co-expression). Recent studies suggest that C2 photosynthetic modification represents a more feasible alternative to full C4 transformation [16,68]. The theoretical and practical advantages of C2 modification are as follows: Model simulations indicate that incorporating the C2 mechanism into C3 crops (e.g., rice) requires fewer structural modifications compared to full C4 transformation. For example, studies on the C2 plant Alloteropsis semialata have shown that C3 and C2 populations differ only in the number of MCs between leaf veins—C2 plants have 3–6 MCs, while C3 plants have 5–11 MCs. Notably, vein density does not differ between C3 and C2 phenotypes of A. semialata, whereas C4 plants exhibit significantly higher minor vein density [78]. All the biochemical genes required for the C2 photosynthetic pathway are already present in C3 species. Therefore, reconstructing the glycine shuttling mechanism requires modifying the regulatory and expression patterns of existing genes. In contrast to C4 transformation, which involves introducing novel metabolic pathways and structural changes, C2 modification necessitates fewer genetic alterations and lower metabolic flux demands, making it a more straightforward approach [68]. Gene editing technologies provide a robust platform for engineering C2 crops. Current research employs two main strategies for C2 transformation: (1) Targeted knockdown of mesophyll GDC H-subunit (GDCH) expression, such as using artificial microRNA (amiRNA) to knock out GDCH expression in rice MCs [79], simulating the reduced GDC activity in C2 plant MCs; and (2) Editing of GDC promoters (e.g., M-box) to preferentially reduce GDC activity in MCs, creating a photorespiration-deficient rice model that mimics C2 photosynthesis [80]. Studies have demonstrated that the M-box promoter region, present in C3-type Moricandia species but absent in C2 types, is key to restricting GDC expression to BSC mitochondria in other C3 plants, providing new possibilities for C2 photosynthetic engineering [16,61]. It should be emphasized that genetic engineering of the C2 pathway poses challenges, including potential metabolic perturbations. For example, limiting GDC expression to BSCs may interfere with metabolite partitioning between mesophyll cells and BSCs, potentially impacting nitrogen metabolism and overall plant growth. Furthermore, the release of ammonia (NH3) during glycine decarboxylation could cause cellular toxicity if reassimilation pathways are impaired.

4.4. Ecological Perspectives on the Resilient Carbon Sink of C2 Photosynthesis

C2 photosynthesis has evolved through convergent evolution in response to declining atmospheric CO2 concentrations, high temperatures, and drought conditions [27,70,81]. Studies suggest that reduced precipitation and increasing temperatures are linked to transitions from C3 to C2 photosynthesis, and from C2 to incipient C4 photosynthesis. While drought, rather than heat, may primarily drive the evolution of C4 photosynthesis, this varies across evolutionary stages, with the initial transition to C2 photosynthesis requiring increased water availability [70]. Compared to C3 plants, C2 plants exhibit higher carbon sink stability and lower photorespiratory losses under high-temperature and high-irradiance conditions [16,68]. Furthermore, C2 plants do not require the complex Kranz anatomy or high energy input necessary for C4 photosynthesis, making them more cost-effective in moderately stressed or resource-limited environments [68]. These traits enable C2 plants to serve as significant carbon sinks in specific ecological niches. Complementary Niche Differentiation: In mixed communities of cotton (C3) and sorghum (C4), CO2 enrichment increases total biomass and leaf area, mitigating the competitive suppression of C3 plants by C4 plants [82]. This suggests that under future elevated CO2 conditions, rational species assemblage within communities can offset the negative impacts of interspecific competition. Although data on the competitive performance of C2 plants in community contexts are limited, niche analysis reveals minimal overlap among C2, C3, and C4 species. For example, in Diplotaxis, the C2-type D. tenuifolia, C3-type D. muralis, and C4-type Cleome gynandra exhibit distinct light saturation point gradients, enabling effective resource utilization across both temporal and spatial niche dimensions. Niche analysis indicates that C2 species typically occupy transitional environments characterized by seasonal rainfall and warm temperatures, bridging the ecological niches of C3 and C4 plants [25]. This distribution often overlaps with savanna habitats, which contribute significantly more to global carbon sinks than temperate forests [83]. Given their evolved ability to adapt to fluctuating precipitation patterns, C2 plants are well-suited to serve as “carbon sink buffers” amid climate change. Notably, in regions impacted by El Niño and La Niña climate phenomena, C3 and C4 plants are highly vulnerable to severe damage, while C2 plants exhibit relatively stronger resilience. Thus, strategically introducing C2 plants to such areas could serve as a cost-effective approach to reducing ecosystem risks and enhancing carbon sink stability. Ecological restoration of marginal lands, such as arid, salinized, and barren soils, presents a global challenge. C2 plants demonstrate superior carbon fixation capabilities in these environments compared to C3 plants, making them promising candidates for ecological restoration projects [25]. Their advantages include high water use efficiency (WUE), efficient carbon assimilation under low CO2 concentrations, and strong adaptability to barren soils, all of which are achieved through optimized nitrogen metabolism [33,63]. Case studies from arid and semi-arid regions further confirm that C2 plants outperform C3 and C4 plants in terms of both adaptability and carbon sink functionality [25].

5. Conclusions

This review systematically examines the mechanistic basis, carbon sink resilience, and potential applications of C2 photosynthesis, drawing the following key conclusions: C2 photosynthesis enhances carbon sink resilience through its photorespiratory carbon pump mechanism, which facilitates CO2 concentration in the BSCs, significantly reduces the CO2 compensation point, and maintains exceptional carbon sink stability under low CO2 levels, high temperatures, and drought conditions. This adaptation exemplifies a sophisticated physiological response, underscoring the evolutionary ingenuity of biological systems [60,66]. C2 photosynthesis demonstrates remarkable convergent evolution across different plant lineages. This photosynthetic pathway plays a vital physiological and ecological role in mitigating the impacts of global climate change and enhancing the carbon sink resilience of the biosphere. The widespread occurrence of C2 photosynthesis across diverse plant families highlights its adaptive response to environmental stressors such as reduced CO2 availability and elevated temperatures [27,70,81]. Compared to C3 and C4 plants, C2 plants exhibit superior carbon sink resilience. Furthermore, C2 modification presents fewer technical challenges than C4 engineering, making it a more technically feasible strategy for enhancing carbon sequestration in both crops and ecosystems. These advantages position C2 photosynthesis as a promising tool for ecological applications, particularly in the management of marginal lands, where factors such as drought and poor soil quality limit the growth of traditional crops. Given the ongoing challenges posed by global climate change, harnessing the resilient carbon sink function of C2 plants presents a practical approach to achieving long-term stable carbon sinks [16,68].
However, despite these advantages, several critical research gaps remain in the study of C2 photosynthesis. Research into the physiological mechanisms underlying C2 photosynthesis is still in its infancy. Further investigation is urgently required in areas such as the regulation of small RNAs, epigenetic modifications, and the precise regulation of gene expression at the genomic level. Such studies are essential to fully understand how C2 photosynthesis operates and how it can be optimized for crop species [53,61]. Moreover, currently available biotechnologies, such as gene editing, high-throughput sequencing, and single-cell sequencing, should be promptly applied to research on the distinct characteristics of the C2 photosynthetic pathway. Although C2 modification is technically less complex than C4 engineering, challenges persist in optimizing the cost-effectiveness, environmental adaptability, metabolic compatibility, and genetic stability of the engineered traits. Overcoming these challenges is crucial for advancing the practical application of C2 photosynthesis in agriculture [68,79]. Ecological research pertaining to C2 plants remains relatively underdeveloped. Further studies are needed to explore the competitive interactions of C2 plants at the individual, community, and ecosystem levels, including understanding both aboveground and belowground interactions and the role of C2 plants in modifying soil microbial communities. These studies will be pivotal in predicting the ecological impacts of introducing C2 plants into various environments and optimizing their carbon sink potential [25,84].
In summary, C2 photosynthesis holds considerable promise as a resilient carbon sink mechanism that could play a significant role in mitigating the effects of global climate change. As research advances, the full potential of C2 photosynthesis for both ecological restoration and agricultural enhancement is likely to be realized.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/biology15010005/s1, Table S1: Comparative Analysis of leaf anatomical feature Across C3, C2, and C4 Species; Table S2: Comparative Analysis of Photorespiration Traits Across C3, C2, and C4 Species; Table S3: Comparative Analysis of Photosynthetic Traits Across C3, C2, and C4 Species under normal condition; Table S4: Comparative Analysis of Photosynthetic Traits Across C3, C2, and C4 Species under stress condition [85,86,87,88,89,90,91,92,93,94].

Author Contributions

J.Z. conceptualized the study and wrote the manuscript. F.C. contributed to the analysis of the literature and editing of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, Grant Number: 32360254.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All data generated or analyzed during this study are included in this published article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Biology 15 00005 g001
Figure 1. A schematic diagram illustrating the primary cellular architecture, key organelles, and core photosynthetic enzymes in the leaves of C3 (a), C2 (b), and C4 (c) plants. Detailed comparative analyses of leaf anatomical structures among the three plant types are provided in Table S1. Abbreviations: MC: Mesophyll cell, BSC: Bundle sheath cell, VTC: Vascular tissue cell.
Figure 1. A schematic diagram illustrating the primary cellular architecture, key organelles, and core photosynthetic enzymes in the leaves of C3 (a), C2 (b), and C4 (c) plants. Detailed comparative analyses of leaf anatomical structures among the three plant types are provided in Table S1. Abbreviations: MC: Mesophyll cell, BSC: Bundle sheath cell, VTC: Vascular tissue cell.
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Figure 2. (a) C3, (b) C2, (c) C4 and (d) CAM subtype photosynthesis.
Figure 2. (a) C3, (b) C2, (c) C4 and (d) CAM subtype photosynthesis.
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Table 1. C2 species by family and lineage.
Table 1. C2 species by family and lineage.
FamilyLineageC2 SpeciesReferences
Monocots
PoaceaeAlloteropsisAlloteropsis semialata[16]
HomolepisHomolepis aturensis, H. isocalycia, H. longispicula[16,17]
NeurachneNeurachne minor[16,18,19]
SteinchismaSteinchisma cuprea, S. decipiens, S. hians, S. spathellosa, S. exiguiflora, S. spathellosum, S. stenophylla[16,17,20,21]
Eudicots
AcanthaceaeBlepharisBlepharis acuminate, B. diversispina, B. espinosa, B. gigantea, B. natalensis, B. nolimetangere, B. sinuate, B. pruinose, B. subvolubilis[16]
AmaranthaceaeAlternantheraAlternanthera cruci, A. ficoidea, A. tenella[16,20]
SalsolaSalsola arbusculiformis, S. divaricate, S. deschaseauxiana, S. gymnomaschala, S. verticillate, S. laricifolia[21,22,23,24]
SedobassiaSedobassia sedoides[16,25]
AsteraceaeFlaveriaFlaveria angustifolia, F. anomala, F. chloraefolia, F. floridana, F. linearis, F. oppositifolia, F. pubescens, F. ramosissima, F. sonorensis[16,20,26,27,28,29,30]
PartheniumParthenium hysterophorus[16,31]
BoraginaceaeHeliotropiumHeliotropium convolvulaceum, H. greggii, H. racemosum, H. lagoense[16,32,33,34]
BrassicaceaeBrassicaBrassica gravinae[16]
DiplotaxisDiplotaxis erucoides, D. tenuifolia, D. muralis[16,35]
MoricandiaMoricandia arvensis, M. nitens, M. suffruticosa, M. sinaica, M. spinosa[16,35,36]
CleomaceaeCleomeCleome paradoxa[16,37,38]
EuphorbiaceaeEuphorbiaEuphobia acuta, E. johnstonii, E.racemosa[39,40,41]
HypertelisHypertelis spergulacea[16]
MolluginaceaeParamollugoParamollugo nudicaulis[41]
MollugoMollugo verticillata[16,26,41]
NyctaginaceaeBougainvilleaBouganvillea cv. Mary Palmer[42]
PortulacaceaePortulacaPortulaca cryptopetala, P. hirsutissima, P. mucronate, P. amillis, P. biloba, P. elatior, P. smallis[16,43,44]
ScrophulariaceaeAnticharisAnticharis ebracteate, A. juncea[16,45]
ZygophyllaceaeTribulusTribulus cristatus, T. astrocarpus[46]
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Zhu, J.; Chen, F. C2 Resilient Photosynthesis: A Practical Option for Long-Term Stable Carbon Sinks? Biology 2026, 15, 5. https://doi.org/10.3390/biology15010005

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Zhu J, Chen F. C2 Resilient Photosynthesis: A Practical Option for Long-Term Stable Carbon Sinks? Biology. 2026; 15(1):5. https://doi.org/10.3390/biology15010005

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Zhu, Junjie, and Fengyue Chen. 2026. "C2 Resilient Photosynthesis: A Practical Option for Long-Term Stable Carbon Sinks?" Biology 15, no. 1: 5. https://doi.org/10.3390/biology15010005

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Zhu, J., & Chen, F. (2026). C2 Resilient Photosynthesis: A Practical Option for Long-Term Stable Carbon Sinks? Biology, 15(1), 5. https://doi.org/10.3390/biology15010005

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