Abiotic stresses, such as drought, salinity, and extreme temperatures, pose significant threats to global agriculture by severely hampering plant growth and reducing crop yields. Climate change has intensified these constraints through more frequent and severe weather events, leading to extensive soil degradation, salinization, and desertification (Prăvălie et al., 2021). Globally, abiotic stress can reduce crop yields by more than 60% and recent estimates attribute 58% of agricultural losses between 2017 and 2022 to natural disasters such as droughts and floods (Boyer, 1982; Daryanto et al., 2016; Webber et al., 2018; FAO, 2023). As the global population is projected to reach 10.3 billion by 2080, improving crop resilience to these environmental pressures is an urgent priority for food security (United Nations, 2025).

Plants activate complex physiological and biochemical adaptations to abiotic stress, including osmotic adjustment, antioxidant activation, and hormonal regulation (Sánchez-Bermúdez et al., 2022; Zhang et al., 2023). Among these adaptive mechanisms, carotenoid-derived apocarotenoids have attracted particular attention for their dual roles as antioxidants and signaling molecules. Under oxidative stress conditions, the degradation of carotenoids produces diverse apocarotenoids that participate in developmental regulation and stress adaptation (Ramel et al., 2012b; Zheng et al., 2021b; Mitra and Gershenzon, 2022; Stra et al., 2023). Classic examples include abscisic acid (ABA) and strigolactones (SLs), which regulate drought tolerance, shoot branching, and root development (Sharp and LeNoble, 2002; Gomez-Roldan et al., 2008; Dodd, 2013; Harris, 2015; Lanfranco et al., 2018; Barbier et al., 2019).

In recent years, β-cyclocitral (β-CC), a volatile aromatic apocarotenoid (2,6,6-trimethyl-1-cyclohexene-1-carboxaldehyde) derived from β-carotene oxidation, has emerged as a conserved signaling molecule across diverse photosynthetic and non-photosynthetic lineages. Beyond its observed roles in vascular plants, β-CC has been detected in cyanobacteria, microalgae, lichens, mosses, and fungi, suggesting that β-carotene cleavage and its signaling derivatives arose early in evolution (Saritas et al., 2001; García-Plazaola et al., 2017; Arii et al., 2021). In fungi, β-CC has been associated with distinctive flavor profiles, highlighting its sensory significance. In single-celled photosynthetic organisms, including cyanobacteria and microalgae, volatile organic compounds (VOCs) such as β-CC mediate cell-to-cell communication (Roach et al., 2022; Zuo, 2023). In bryophytes, β-CC has been implicated in allelopathic interactions, where moss or lichen extracts influence neighboring bryophytes or vascular plants (Vicherová et al., 2020; Matić et al., 2024). Within higher plants, β-CC participates in photooxidative stress mitigation, root architecture modulation, and herbivore deterrence, while also triggering programmed cell death and detoxification pathways under high-light or oxidative stress conditions (Zorn et al., 2003; García-Plazaola et al., 2017; Roach et al., 2022; Zuo, 2023; Wang et al., 2024).

Complementing these functions, the oxidized and water-soluble derivative β-cyclocitric acid (β-CCA) has recently been identified as a downstream product of β-CC oxidation in planta (D’Alessandro et al., 2019; Braat et al., 2023). β-CCA accumulates under drought and light stress and retains signaling activity, activating detoxification and cell-cycle regulators such as SCL14 and SMR5. Together, β-CC and β-CCA form a metabolic and signaling continuum that connects carotenoid oxidation to redox balance, growth modulation, and environmental adaptation across taxa. This evolutionary conservation underscores that β-CC is not merely a by-product of carotenoid degradation but a pivotal mediator of cellular communication and stress resilience throughout the plant kingdom and beyond.

Together, these observations highlight β-CC and its oxidized derivative β-CCA as evolutionarily conserved mediators of stress signaling, spanning photosynthetic and non-photosynthetic organisms alike. Despite increasing evidence of their diverse physiological roles, the biochemical origins and signaling dynamics of these molecules remain incompletely resolved. A clearer understanding of how β-CC is generated, interconverted with β-CCA, and incorporated into plant stress networks is therefore essential for interpreting their functions across species. The following sections synthesize current knowledge on the biosynthetic pathways and regulatory mechanisms underlying β-CC production and signaling, providing a framework for its potential integration into crop stress-adaptation research.

Carotenoids comprise a diverse group of over 750 lipophilic isoprenoid pigments characterized by a C₄₀ backbone with conjugated double bonds (Cuttriss et al., 2011). This unique structure confers both photoprotective capabilities and oxidative susceptibility. In photosynthetic organisms, carotenoids serve essential roles in light absorption within the blue-green spectrum and excited chlorophyll state quenching via electron transfer, while also functioning as antioxidants and contributing to pigmentation (Mozzo et al., 2008; Hashimoto et al., 2016; Sun et al., 2022). Their structural reactivity enables oxidative cleavage into bioactive apocarotenoids through two primary pathways: enzymatic and non-enzymatic (Figure 1).

The enzymatic pathway centers on carotenoid cleavage dioxygenases (CCDs), which mediate specific oxidative cleavage by inserting oxygen atoms between carbon-carbon double bonds (Giuliano et al., 2003; Hou et al., 2016). This evolutionarily conserved non-heme iron enzyme family exhibits substrate promiscuity, with substrate isomerization sometimes required for oxidation (McQuinn et al., 2015). In Arabidopsis, nine CCD family members demonstrate functional specialization: NCEDs convert 9-cis-violaxanthin/neoxanthin to xanthoxin (ABA precursor) (Nambara and Marion-Poll, 2005); CCD7/8 sequentially cleave substrates for strigolactone biosynthesis (Alder et al., 2012); while CCD4 isoforms generate flavor/aroma compounds in tissue-specific patterns (Rubio-Moraga et al., 2014). Gene duplication events, exemplified by the discovery of CCD2 in Crocus sativus, drive functional diversification within the CCD family (Frusciante et al., 2014). Cleavage site preferences of various CCDs have been well defined: CCD1 targets 9.10 positions, CCD2 specifically cleaves at 7,8 sites near β-ionone rings, while CCD4 exhibits dual positional specificity (Vega-Teijido et al., 2019).

Nonenzymatic oxidation occurs primarily under oxidative stress, where reactive oxygen species drive nonspecific carotenoid degradation. In chloroplast reaction centers, spatial separation prevents β-carotene from quenching excited chlorophyll (³Chl), leading to singlet oxygen (¹O₂) generation that randomly oxidizes carotenoid backbones into volatile aldehydes and ketones (Ramel et al., 2012a). Lipoxygenases like TomLoxC in tomato further contribute to this process by oxidizing β-carotene despite their primary role in fatty acid metabolism (Hayward et al., 2017; Gao et al., 2019).

Collectively, these pathways demonstrate that β-CC originates both as a regulated metabolic signal and as a stress-induced oxidation product. The evolutionary conservation of core CCD enzymes across plant lineages, particularly the CCD4 and NCED clades, suggests broad potential for cross-species applications, though functional divergence in non-model species necessitates careful examination. An overview of β-carotene-derived apocarotenoids, their associated cleavage enzymes, and their characterized biological roles across taxa is summarized in Table 1.

Because β-CC formation is tightly coupled to carotenoid turnover and reactive oxygen dynamics, its synthesis links photosynthetic metabolism directly to stress perception. This biochemical connection provides the foundation for its role as a mobile signaling molecule that conveys chloroplast-derived oxidative cues to other cellular compartments. Understanding how these biosynthetic events translate into downstream signaling is therefore essential for elucidating the physiological relevance of β-CC. The following section discusses current evidence for β-CC-mediated signaling under abiotic stress and its emerging role in coordinating plant adaptive responses.

β−CC elicits diverse stress-responsive signals, enhancing plant survival under unfavorable conditions. A central component of abiotic stress responses is the production and accumulation of reactive oxygen species (ROS). While traditionally viewed as toxic byproducts of stress, ROS are now recognized as key signaling molecules that mediate retrograde signaling, where chloroplast-originated signals influence nuclear gene expression.

In Arabidopsis, hydrogen peroxide (H₂O₂) production via NADPH oxidases initiates signaling cascades from the plasma membrane that ultimately trigger antioxidant defenses (Ma et al., 2012; Ben Rejeb et al., 2015a, 2015b). Calcium influx and the generation of an electrochemical gradient further amplify ROS signals throughout the plant (Gilroy et al., 2016). This leads to the activation of stress-responsive transcription factors, including members of the WRKY and MYB families (Mabuchi et al., 2018; Naing and Kim, 2021; Zheng et al., 2022; Javed and Gao, 2023). Notably, singlet oxygen (¹O₂), one of the most reactive forms of ROS, is unlikely to act directly as a signaling molecule due to its extremely short half-life and membrane impermeability. β−CC has been identified as a likely secondary messenger, transmitting the signal initiated by ¹O₂.

Recent studies support the role of β−CC as a retrograde signal that can migrate from the chloroplast to other cellular compartments (Chi et al., 2015; Chan et al., 2016; D’Alessandro and Havaux, 2019). Other retrograde signaling molecules, such as 3′-phosphoadenosine 5′-phosphate (PAPS) and dihydroxyacetone phosphate (DHAP), require specific membrane transporters (Vogel et al., 2014; Wang et al., 2020; Ashykhmina et al., 2022). In contrast, β−CC is a small, volatile, and lipid-soluble molecule that can potentially diffuse freely across membranes. This property allows β−CC to function as a mobile signal during abiotic stress responses. Nevertheless, the precise mechanism by which β−CC is transported, and the identity of its primary molecular targets remain unclear.

Figure 2 summarizes the current understanding of β-CC-mediated responses under different abiotic stress conditions, as well as its regulatory influence on root development. The following subsections discuss these processes in detail, emphasizing the molecular and physiological mechanisms through which β-CC contributes to plant stress tolerance.

The signaling functions of β-CC and its oxidized derivative β-CCA have been characterized across diverse plant taxa, including Arabidopsis, rice, tomato, and peach. These studies collectively reveal conserved pathways that link carotenoid oxidation with stress signaling, redox regulation, and developmental reprogramming. The apparent conservation of β-CC–mediated pathways across monocots and dicots suggests that similar mechanisms may operate in other crops where this signaling has yet to be explored. Among these, soybean (Glycine max) represents a particularly promising system for translational application. As a globally important legume highly sensitive to drought, salinity, and photooxidative stress, soybean provides an ideal model for testing whether apocarotenoid signaling can be harnessed to enhance abiotic stress tolerance in economically relevant species.

Soybean (Glycine max L. Merr.) ranks among the world’s most widely cultivated legumes, producing over 370 million metric tons annually across 136 million hectares (FAO, 2025). Beyond its role as a major source of plant protein and oil, soybean contributes to agricultural sustainability through symbiotic nitrogen fixation, improving soil fertility and reducing dependence on synthetic fertilizers (Liu et al., 2021; Alves et al., 2024; Yan et al., 2024). However, soybean growth and productivity are highly sensitive to environmental fluctuations. Photoperiod, temperature, and water availability remain key determinants of yield potential (Major and Johnson, 1974; Major et al., 1975b, 1975a). Moreover, a large proportion of global soybean cultivation is rainfed, making the crop especially vulnerable to climate variability (Barrera et al., 2025). Drought stress during reproductive stages can result in yield losses exceeding 70–80% when water deficits coincide with flowering and pod filling (Poudel et al., 2021; Nguyen et al., 2023; Ferreira et al., 2024). With increasing drought frequency and intensity projected under future climate scenarios, developing soybean cultivars with improved stress resilience is an urgent priority.

Traditional breeding has enhanced yield and quality traits, but the polygenic and environment-dependent nature of abiotic stress tolerance has limited rapid genetic gains. Complex genotype-by-environment interactions, coupled with the slow progress of conventional selection, have prompted growing interest in biotechnological and physiology-based approaches that leverage new insights into plant signaling and metabolism (Mohapatra et al., 2024; Mushtaq et al., 2025; Prasanna et al., 2025; Vieira et al., 2025). In this context, β-CC has emerged as a potential signaling molecule of agronomic relevance due to its ability to modulate key stress response networks in model species.

Mechanistic studies have shown that β-CC enhances drought tolerance independently of classical ABA signaling while modulating root system architecture through pathways partially analogous to those of SLs. Its oxidized derivative, β-CCA, adds another regulatory layer through activation of the SCL14-dependent detoxification pathway and modulation of cell-cycle regulators such as the cyclin-dependent kinase inhibitor SMR5 and downstream ANAC transcription factors (D’Alessandro et al., 2019; Braat et al., 2023). Comparative genomic analyses indicate that soybean possesses orthologs corresponding to many of these regulatory genes identified in Arabidopsis and other species (Table 2). The functional characterization of these orthologs, such as GmMBS1, GmSCL14, GmSMR5, and GmCYP81D11, remains an important gap and represents a critical next step toward translating β-CC and β-CCA signaling research into legume systems.

Despite the central role of carotenoid metabolism in plant stress physiology, carotenoid cleavage dioxygenases (CCDs) remain underexplored in soybean. Current evidence primarily concerns GmCCD1 and GmCCD4, whose expression has been linked to lutein turnover, floral pigmentation, and responses to abiotic stresses including salinity and heat (Kanamaru et al., 2009; Wang et al., 2013; Gao et al., 2020). GmCCD4 shares structural features with CsCCD4 from Crocus sativus, but its possible involvement in generating β-CC or related apocarotenoids under stress remains unknown. Systematic functional and biochemical analyses of the soybean CCD family will therefore be essential for elucidating the enzymatic sources of β-CC and clarifying whether its biosynthesis mirrors that observed in other crops.

Beyond genetic and molecular avenues, β-CC and β-CCA also hold potential as exogenous treatments or seed-priming agents to improve early seedling vigor under stress. Studies in model plants demonstrate that β-CC pretreatment enhances germination and seedling establishment under osmotic or oxidative stress, indicating possible utility for improving soybean emergence and early growth in drought-prone environments (Dickinson et al., 2019; D’Alessandro et al., 2019; Deshpande et al., 2021a; Braat et al., 2023). Recent work by Hazra et al. (2025) further strengthens this concept by showing that β-CC acts as a signaling molecule that extends seed longevity in Arabidopsis. Their results revealed that apocarotenoids, rather than carotenoids themselves, govern seed viability: double mutants lacking CCD1 and CCD4 displayed sharply reduced longevity, whereas exogenous β-CC application restored viability even under accelerated aging. β-CC treatment reduced lipid peroxidation and hydrogen-peroxide accumulation while enhancing antioxidant enzyme activity, including ascorbate peroxidase and catalase. Notably, β-CC and β-ionone directly activated expression of the tonoplast aquaporin TIP2;2, a protein essential for ROS detoxification during seed storage. Together, these findings demonstrate that β-CC contributes to seed vigor and redox stability through apocarotenoid-dependent signaling rather than pigment accumulation, highlighting its potential as a natural seed-conditioning compound for enhancing germination and longevity under adverse conditions.

Furthermore, β-CC’s influence on root architecture is of particular relevance to leguminous crops. Root growth and nodule formation are central to symbiotic nitrogen fixation, yet both processes are highly sensitive to drought and salinity (Singleton and Bohlool, 1984; Duzan et al., 2004; Kunert and Vorster, 2020; Lumactud et al., 2023). β-CC’s reported capacity to promote root branching and elongation under stress suggests potential to maintain nodulation and nitrogenase activity when water availability is limited. Future research should evaluate how β-CC treatments affect root exudation profiles, nodule initiation, and nitrogen assimilation efficiency under abiotic stress, integrating these physiological responses with molecular markers of apocarotenoid signaling.

While the economic feasibility of β-CC and β-CCA application in field conditions remains to be determined, their biological activity at nanomolar to micromolar concentrations and natural occurrence suggest a low risk of harmful residues. Nonetheless, the lack of residue data in edible tissues represents a critical knowledge gap. Compared with synthetic hormone analogs such as ABA derivatives, β-CC offers a potentially safer and more sustainable approach. Advances in microbial production systems, such as β-CC biosynthesis in engineered cyanobacteria, could further reduce costs and environmental impact, though technical scale-up and regulatory validation remain key challenges before commercial deployment.

Despite significant advances in our understanding of carotenoid-mediated stress responses, substantial gaps remain that hinder the translation of apocarotenoid biology, particularly β−CC and its derivative β−CCA, into agricultural applications. One of the foremost challenges is the incomplete elucidation of β-CC signaling mechanisms. While its association with detoxification pathways and developmental reprogramming under abiotic stress is increasingly evident, the identity of its receptors, the specificity of its tissue-level responses, and the extent of its interaction with canonical phytohormones such as ABA, SLs, brassinosteroids, salicylic acid, and ethylene remain unresolved. A multiomics framework that integrates transcriptomic, proteomic, and metabolomic analyses, coupled with CRISPR-based functional validation, will be essential to clarify these hierarchical relationships and decode the broader β-CC–responsive network across plant systems.

The lack of translational validation of β−CC in economically important crops is also critical. To date, functional characterizations of β−CC and β−CCA have been conducted in Arabidopsis a few model or horticultural species, with limited extension to cereals, legumes, and other agronomically important plants. Although homologs of β−CC-responsive genes are widely conserved, including those encoding MBS1, SCL14, SMR5, and CYP81D1, their specific roles in crop stress adaptation remain to be tested under field conditions. Similarly, the CCD and SMR gene families which are central to β−CC biosynthesis and signaling have been only partially explored in crops such as soybean, maize, and wheat, leaving key regulatory nodes functionally uncharacterized.

Developing scalable and field-applicable delivery systems for β CC remains a significant challenge. Current methods of exogenous application are largely experimental and constrained by the compound’s volatility, short half-life, and instability under environmental conditions. To fully harness β CC’s potential, especially its pronounced effects on root architecture, more targeted and sustainable delivery strategies must be developed. Rhizosphere-focused approaches are particularly promising. For instance, algal biofilms have been explored as biodegradable soil amendments capable of delivering bioactive compounds directly to the root zone while simultaneously improving soil structure and microbial diversity (Gonçalves et al., 2023; Gurau et al., 2025). Likewise, nanoencapsulation technologies can stabilize the controlled release of β CC, while engineered microbial consortia could be designed to produce or release β CC in a root-proximal, stress-responsive manner (Moradipour et al., 2019; Balla et al., 2022; Szopa et al., 2022).

The potential impact of β-CC on legume symbioses warrants particular attention. Its documented effects on root growth and stress signaling suggest possible roles in regulating nodule initiation, function, and communication with Bradyrhizobium species. Given the importance of symbiotic nitrogen fixation to legume productivity and soil health, elucidating how β-CC modulates these interactions could significantly advance its application in sustainable crop management.

While β-CC and β-CCA represent versatile signaling molecules capable of enhancing plant resilience to multiple stresses, their broad physiological effects necessitate careful evaluation of developmental and ecological trade-offs. For example, modulation of root morphology may alter rhizosphere microbial community structure, influencing beneficial associations such as nitrogen fixation or mycorrhizal colonization. Moreover, genetic manipulation of CCD activity to increase β-CC production must be balanced against potential depletion of carotenoid pools essential for photoprotection and photosynthetic stability.

Ensuring that β-CC-mediated adaptations are both effective and ecologically sustainable will require multi-environment validation and long-term systems-level assessment. Field trials integrating physiological, molecular, and agronomic data should evaluate trait stability, metabolite persistence, and effects on nutrient cycling and soil microbial dynamics. Ultimately, realizing the translational potential of β-CC and β-CCA will depend on close collaboration among plant physiologists, molecular biologists, breeders, and agronomists. Through such interdisciplinary efforts, apocarotenoid signaling could become a foundation for developing climate-resilient and resource-efficient crops.

β-CC and its oxidized derivative β-CCA have emerged as key apocarotenoid signals that integrate oxidative stress perception, detoxification, and developmental regulation across diverse plant taxa. Their conserved roles in modulating photosynthetic stability, antioxidant defense, and root plasticity highlight their importance as central mediators of abiotic stress adaptation. The growing body of evidence underscores their potential as natural biostimulants and molecular targets for engineering stress-resilient crops. Yet, realizing this potential will require translational validation in field environments, functional characterization of key signaling components in major crops, and ecological assessments to ensure sustainability. Harnessing β-CC-mediated signaling thus represents a promising step toward developing climate-resilient, resource-efficient agricultural systems.