Plant agency: from senome and electrome to plant semiosphere

1 Introduction: towards plant agency

Historically, plant life has been constrained by reactive paradigms that restrict biological agency to complex brains. Inheriting the Aristotelian ‘vegetative soul’, botany restricted plants to growth and reproduction, devoid of sensation or movement (Aristotle, 1957; Hall, 2011, p. 37; Marder, 2012; Gagliano, 2013). This passivity was reinforced by the convergence of Newtonian mechanicism and Cartesian dualism. While Newton provided a deterministic framework of action and reaction (Mazzocchi, 2008; Noble, 2012; Bongard and Levin, 2021), Descartes bifurcated reality into res cogitans and res extensa, postulating that isolated parts explain the whole and framing the living being as an ‘organic machine’ (Descartes, 2006; Mazzocchi, 2008; Noble, 2012; Baluška and Reber, 2021a). Consequently, a cerebrocentric bias emerged: modern science replaced the soul with the centralized nervous system as the sole seat of agency, relegating plants to automata devoid of interiority or purposeful behavior (Trewavas, 2005a; Calvo, 2016; Baluška and Reber, 2021a).

In opposition to this strictly reactive view, contemporary experimental evidence demonstrates that plants exhibit complex capacities for anticipation (Shemesh et al., 2010; Calvo and Friston, 2017), memory (Thellier and Lüttge, 2013; Crisp et al., 2016), learning (Gagliano et al., 2014; Souza et al., 2018), and decision-making (McNickle and Cahill, 2009; Souza et al., 2017). These findings expose the conceptual limitations of the classical model and indicate that the plant organism operates as an agent endowed with integrated cognitive complexity (Trewavas, 2003, Trewavas, 2005b; Calvo, 2016). Thus, the classical dominant paradigm in natural sciences ignores the possibility that life is not an assembly of inert components but an uninterrupted lineage of “sentience”. Since membrane excitability and cytoplasmic organization are continuously inherited in each cell division, sentience and agency are intrinsic attributes of the structural continuity of life, making it impossible to reduce the organism to an automaton devoid of interiority (Baluška et al., 2024).

However, behavioral observations alone are insufficient to ground a biological theory. We must investigate the biophysical foundations at the elementary level of life (the cell) to understand how agency manifests and articulates across different biological scales (the plant). Starting from the need to establish an elementary grounding, this article proposes a synthesis based on the theoretical perspective of Cellular Cognitive Biology (Baluška et al., 2024), where agency is an intrinsic and coterminous attribute of life, sustained by the cellular senome (Baluška et al., 2022). The senome acts as an analog and multimodal biophysical field that integrates bioelectric (electrome), bioelectromagnetic, and mechanical dynamics, functioning as the primary interface of sentience (Baluška and Miller, 2018) and provides the support for the plant’s agency, defined here as the capacity for self-determination and persistence against entropic degradation. On this basis, intentionality emerges as goal-directedness, where sentience mediated by senoma drives motor intentions, directing the plant (both roots and shoots) toward a world perceived as a field of potential metabolic fulfillment (Husserl, 1982; Wang et al., 2021). This is grounded in the ‘primordial metabolic concern’ (Jonas, 1966; Marder, 2012) for ‘expected inputs’ (i.e., resources like light and nutrients that “complete” the plant). Consequently, sensing is inseparable from agency, as specific interactions ensure structural continuity. By interpreting these interactions as processes of semiosis (Peirce, 1958), the plant translates biophysical sentience into meaning. Through semantic couplings, the plant projects agency into its niche, converting physical signaling into qualitative signs with value and purpose for life maintenance (Kull, 2000; Witzany, 2008).

By integrating the multimodal dynamics of the senome with a semiotic matrix, we establish the foundations of agency at the organismic scale. This allows us to understand how plant agency scales from individual cells to semi-autonomous modules, and how these units integrate to generate the agency of the whole plant as a unified system of navigation in the world. Consequently, the purpose of this work is to elucidate the theoretical foundation explaining how plant agency emerges from the coordination between multiple functional units, interpreting plant organization as a network of communicative cooperation (zu Castell et al., 2019). This process represents an integrative emergence (Lüttge, 2022), where modules are self-organizing agents that unify into a higher-order system of sentience. By grounding this scalar transition, we offer a perspective that investigates plant life not as a set of isolated mechanisms, but as a continuous process of agency ensuring persistence of organismal identity across increasingly complex biological scales (Baluška, 2025).

2 Organizational logic: autopoiesis and the enactive nature of agency

Biological agency finds its foundation in the logic of autopoietic organization, which defines living beings as systems capable of producing and maintaining their own identity through a continuous network of transformations (Maturana and Varela, 1980; Luisi, 2003). Unlike technical artifacts, which have externally imposed purposes, organisms operate as ‘Kantian Wholes’, where every part exists for the whole and the whole exists through the parts in a reciprocal causality (Baluška, 2025; Baluška et al., 2026). In these systems, the absence of a privileged level of causality implies that agency is not concentrated in a specific command center, but emerges from the horizontal coordination of all components. In a plant, this means that roots, shoots, and leaves are not merely assembled components, but mutually constitutive organs that produce and sustain each other through integrated metabolic work. This organization requires the closure of constraints and catalytic cycles, allowing the system to perform continuous thermodynamic work to sustain its structure against the dissipative tendency of entropy (Miller et al., 2024).

Because biological organization is inherently decentralized, plant cognition cannot be an abstract or centralized processing of data; instead, it must be an embodied and enactive process, where “awareness” of the world emerges from the active interaction of the expanding body with its surroundings. By proposing that cognition is a property of integrated and dynamic systems, this perspective rejects ‘brain chauvinism’ (Varela et al., 1991; Newen et al., 2018), effectively opposing the premise that cognition strictly requires a centralized processing unit. Since the plant lacks a privileged neural center, its cognitive agency manifests as a relational and distributed property, resulting from the communicative coordination between its semi-autonomous modular units and their respective senomes. This enactive sense-making is best illustrated by Jakob von Uexküll’s functional cycle (Funktionskreis), which in plants is uniquely driven by indeterminate growth. As a root tip cognitively navigates through soil heterogeneity (Baluška et al., 2009, Baluška et al., 2021), it does not merely react to nutrient gradients; it actively expands its subjective world (Umwelt) by making sense of its environment based on its metabolic needs (von Uexküll, 2014; Kull, 2000). By acting simultaneously as a sensing and motor organ, the root tip converts physical cues into biological signs, where each growth increment represents a step in the continuous construction and expansion of the plant’s meaningful domain.

Consequently, metabolism ceases to be a mere biochemical description and becomes the phenomenological expression of the ‘primordial concern’ of the living being with its own existence (Jonas, 1966; Barbaras, 2010). Metabolic intentionality manifests in the plant’s relentless effort to manage flows of energy and matter (i.e., seeking the ‘expected inputs’ like light and nutrients that “complete” its biological being) characterizing what is defined as ‘needful freedom’ (Jonas, 1966). This metabolic drive ensures that every physiological process is not a passive reaction, but an activity oriented toward the stability and persistence of the system (Brenner et al., 2006; Trewavas and Baluška, 2011; Trewavas, 2016). As cellular units integrate their activities through catalytic cycles of metabolic networks based on charged biomolecules (Jelen et al., 2016; Lane, 2022), individual cellular “worlds” coalesce into a modular, yet unified, distributed agency of the plant body. Agency emerges, therefore, from the intrinsic need of all cell-based organisms to actively manage environmental perturbations to ensure its structural integrity and persistent navigation across biological scales (Goldenfeld and Woese, 2011; Walsh, 2015; Reber et al., 2023, Reber et al., 2026; Miller et al., 2026a, Miller et al., 2026b).

3 The “infrastructure” of sentience: the senome-electrome ontology

The transition from organizational logic to effective agency requires a multimodal biophysical infrastructure defined as the cellular senome (Baluška and Miller, 2018). The senome acts as an integrative information field that unifies the activities of all the cell’s sensory proteins, functioning as the analog interface between the internal state and the environment (Miller et al., 2020; Baluška and Reber, 2021a). At the core of this structure, the electrome plays the fundamental role of rapid signaling and systemic coordination through variations in membrane potentials and ionic flows (De Loof, 2016; Baluška et al., 2024). In this context, the electrome represents the macroscopic manifestation of the integration of multiple cellular senomes, acting as the constitutive medium of the plant’s subjective world. In plants, this electrical activity is not merely a byproduct of ionic flux dynamics, but a high-capacity information channel. Studies have demonstrated that these signals exhibit complex non-linear dynamics, providing evidence for a sophisticated form of systemic integration (Souza et al., 2017; Saraiva et al., 2017). Unlike the genome (digital and past-focused), the senomic-electrome operates in the analog domain of the present at the nanoseconds-microseconds to milliseconds-seconds time-scale. This analog nature allows for a continuum of intensity and significance, providing the necessary resolution for the emergence of semiotic interpretation and allowing the cell to perform real-time valence evaluations of environmental conditions (Debono and Souza, 2019).

The organism’s capacity to extract relevant information from the environment is grounded in the activity of sensory proteins that operate as biological Maxwell’s demons (Baluška et al., 2022). These sensors convert physical perturbations into chemical and electrical signals, allowing the system to perform anti-entropic work oriented toward survival goals (Nick, 2024; Baluška et al., 2026). This evaluative process represents the emergence of a semiotic threshold, where raw physical perturbations are no longer merely “data” to be transmitted, but are integrated as functional information that carries biological valence for the system’s maintenance. The integration of these signals into the electrome provides the support for ephaptic coupling and communication between cells (Baluška and Reber, 2021a), utilizing the plant’s vascular system as a substrate for long-distance coordination. This process unifies individual responses into a coherent organismic agency (Cervera et al., 2020; Baluška et al., 2022). In this way, the electrome is not merely a byproduct of metabolism but the cognitive interface that allows the living being to navigate fields of bioelectric significance. This infrastructure enables cellular sentience to scale up to the agency of the individual plant, where the system’s stability is maintained by constant sensory vigilance and active self-regulation (Debono and Souza, 2019; Miller et al., 2024; Baluška, 2025).

4 Semiosphere and extended agency: the projection of sentience into the environment

Biological agency does not end at the physical boundaries of the organism, projecting itself into the surroundings through extended cognition processes that configure the ‘Ariadne’s thread’ of plant sentience (Parise et al., 2020, Parise et al., 2023; Marder and Parise, 2024). According to the complementarity principle, plant cognition integrates environmental resources as functional extensions of its biological system, operating in a recursive structural coupling with its niche (Newen et al., 2018; Parise and Marder, 2024). In this context, the cytoskeleton acts as a susception interface dedicated to mechanotransduction, where cortical microtubules and actin filaments function as susceptors that translate environmental mechanical fluctuations from the soil matrix into senomic signaling (Baluška and Mancuso, 2019; Nick, 2024).

For instance, an operational continuity exists between the network of cytoplasmic tensions and the geometry of the soil, given that while mechanical pressures shape the internal architecture of the cell, the organism projects its agency to actively transform the physical substrate through niche construction (Odling-Smee et al., 2003; Laland et al., 2015). Through root growth, the plant modifies the soil’s porosity and water retention capacity, establishing facilitation trails that guide the system’s development (Odling-Smee et al., 2003; Sultan, 2015; Parise and Marder, 2024). This physical modification is accompanied by the active secretion of root exudates and the emission of volatile organic compounds (VOCs), which constitute an external systemic coordination infrastructure (Parise and Marder, 2024). Far from being mere metabolic waste, root secretions actively recruit symbionts, such as arbuscular mycorrhizal fungi, which effectively expand the organism’s perceptual and absorptive capacity (Simard, 2018; Baluška and Mancuso, 2021; Parise et al., 2025). Simultaneously, the plant saturates the air around it with VOCs to create a ‘cognitive atmosphere’ that triggers systemic priming, sustaining a state of physiological alertness in both the emitting individual and neighboring plants (Baldwin et al., 2006; Heil and Kost, 2006; Baluška and Mancuso, 2021; Lucho et al., 2026). From this perspective, the structured soil and chemical atmosphere cease to be inert supports and become a form of embodied, although transitory, spatial memory or environmental inscription. This eco-memory allows the agent’s historical experience to remain registered in the niche configuration, functioning as a persistent guide that channels future behavior and optimizes resource exploration (Sultan, 2015; Trewavas, 2016; Parise et al., 2023; Parise and Marder, 2024).

The union of these mechanical and chemical projections establishes the foundations for the plant semiosphere, comprising the totality of signs created and perceived by the organism, which constitutes the relational domain where biophysical signaling is converted into semantic couplings (Kull, 2000; Hoffmeyer, 2008). As plants represent the only multicellular organism living both in the atmosphere and pedosphere (Baluška and Mancuso, 2021), their semiosphere is embracing very significant space which is relevant for the Earth climate. In the semiosphere, plant intentionality becomes literalized in space, as the living being extends its sentience outside the body to create a habitable and intelligible world. In this scenario, communication assumes the role of a dynamic process of meaning co-creation, where physical, chemical, and biotic elements acquire qualitative value for the system (Kull, 2000; Witzany, 2006). By inhabiting and cocreating this semiosphere, the plant establishes an interpretive link that configures co-intentionality, allowing multiple agents to coordinate their intentions and actions in a world of shared meanings (Marder, 2012; Baluška et al., 2024). This relational activity ensures the system’s persistence through communication networks that connect the individual to higher biological scales, transforming cellular sentience into a phenomenon of distributed agency (Baluška, 2025; Miller et al., 2024, Miller et al., 2026a, Miller et al., 2026b).

5 The holobiont and the N-space episenome: a distributed network agency

Broadening plant agency culminates in the concept of the holobiont, understood as a multilevel biological unit where identity emerges from a mesh of semiotic couplings that transcend the individual organism (Gilbert et al., 2012; Vandenkoornhuyse et al., 2015; Debono and Souza, 2019; Lüttge et al., 2022). In this system, communication acts as the fundamental integrating principle, functioning as the interpretive link that unifies multiple beings into a unit of relational agency. Intentionality, therefore, ceases to be an isolated property of the host and emerges from the network of interactions between multiple biological agents (e.g., plant, fungi, and bacteria), where control and decision-making are shared. This shared agency is evidenced by diverse biological scales: from the ‘biological market’ dynamics and reciprocal rewards in mycorrhizae (Kiers et al., 2011) and the post-infection sanctions used by legumes to manage rhizobial cooperation (Denison, 2000), to the forest-scale mycorrhizal networks that facilitate interspecific communication, learning, and memory (Simard, 2018; Parise et al., 2025). Such networks allow the community to act as a single, coordinated physiological unit that redistributes resources, such as massive interspecific carbon transfer, based on collective needs, effectively converting individual responses into a distributed survival strategy (Klein et al., 2016). This dynamic of self-organization allows the holobiont to operate as a distributed autopoietic system, whose survival capacities scale to the planetary dimension through the Gaia Hypothesis (Lovelock, 1995; zu Castell et al., 2019; Baluška et al., 2026).

The biophysical basis of this integration resides in the N-space episenome, an information matrix that unifies cellular space-time through the overlap of bioelectric fields and ephaptic interactions (Miller et al., 2020; Baluška and Miller, 2018). When the individual senomes of different species couple, they give rise to the hypersenome, an expanded sphere of sentience that integrates the cognition of the host and its symbionts (Baluška, 2025). In this context, mycorrhizae function as true sensory prostheses, extending plant perception for kilometers and allowing the hypersenome to process environmental information at a scale inaccessible to the isolated individual (Parise and Marder, 2023). Through this coupling, relational agency allows the system to resolve complex ecological problems, converting biotic communication into a collective survival totality.

This perspective requires a revision of evolutionary theory, suggesting that the subject of selection is not just the gene or the individual, but the cognitive agency of populations and communities (Corning, 2023). As predicted by the stress gradient hypothesis, the transition from competitive interactions to facilitation relationships demonstrates that the holobiont is capable of reassessing the environmental context through shared sensory vigilance (Bertness and Callaway, 1994; He et al., 2013). Evolution, therefore, is guided by cognitive selection, where social processes and semiotic flows in the N-space act as the architects of biological trajectory (Miller et al., 2024; Baluška et al., 2026). By understanding plant communities as units of distributed agency, we reveal that life is maintained by a continuous network of meanings that ensures systemic resilience against global entropy (zu Castell et al., 2019; Baluška, 2025; Baluška et al., 2026).

6 Theoretical synthesis: from senomic coupling to holobiont agency

The convergence between the biophysics of cellular sentience and the semiotics of systemic agency suggests that the infrastructure of plant communication is sustained by the indissoluble union between senomic coupling and semantic coupling. Senomic coupling, based on the physical overlap of bioelectromagnetic fields, ephaptic interactions, and mechanical vibrations, provides the necessary interface for the unification of informational space-time in what is defined as the N-space episenome (Miller et al., 2020; Baluška and Reber, 2021b). This biophysical base supports the manifestation of co-intentionality, where the exchange of signals ceases to be a mechanical event and is processed as an active grammar of meaning and purpose (Nick, 2024; Marder, 2012; Baluška et al., 2024).

In this context, plants and their symbionts operate as ‘Kantian Wholes’, performing continuous thermodynamic work to convert metabolic necessity into a relational agency that projects the organism into its semiosphere (Baluška et al., 2022; Miller et al., 2024; Baluška et al., 2026). The transition from the individual senome to the hypersenome of the biosphere represents the maximum scale of this integration, where life is maintained by a network of eco-memories and environmental inscriptions that ensure global homeostasis through cognitive self-regulation (Baluška, 2025).

This synthesis proposes that plant behavior is a process of navigation in an integrated field of meaning, culminating in the organization of the holobiont as a functional evolutionary unit, capable of enacting its niche and its collectivity.

7 Implications and future perspectives

Expanding the agency paradigm towards its relational and distributed dimensions necessitates a profound revision of scientific and social practices. Methodologically, this requires the development of non-invasive monitoring and complex systems analysis that respect the communicative nature and temporal scales of plants (Witzany and Baluška, 2012). In agriculture, this perspective redefines the rhizosphere not as a mere nutrient reservoir, but as a functional component of a complex cognitive-metabolic network. Recognizing the soil-root interface as an extension of plant agency allows for the transition from mechanical manipulation to process-oriented ecological management, prioritizing niche construction and systemic facilitation over external chemical control.

Ethically, the recognition of plant intentionality challenges the core of anthropocentrism and demands a reconciliation between ontology and ethics (Oliveira, 2024). If the plant, through its metabolic striving, affirms its own existence against non-being, it irrefutably establishes that life is an intrinsic “good” (Oliveira, 2024). This realization imposes a duty of responsibility upon us as guardians of an alterity that we have historically silenced. Overcoming ‘plant imperception’ is, therefore, a pedagogical and moral imperative; it requires abandoning the view of the biosphere as res extensa (i.e., a mere storehouse of resources) and recognizing our belonging to a shared autopoietic web.

The study of distributed plant agency provides the scientific foundation for a new biocivilization based on global homeostasis and the recognition of the hypersenome that sustains life on Earth. By integrating these relational perspectives, we offer the necessary support for environmental law to evolve toward the recognition of ecosystems as legal subjects, ensuring a future grounded in semiotic cooperation and systemic resilience (Baluška and Mancuso, 2020; Slijepčević, 2023, Slijepčević, 2024; Oliveira, 2024; Miller et al., 2024; Baluška, 2025).

Generative AI statement

The author(s) declared that generative AI was used in the creation of this manuscript. For text/English correction.

Any alternative text (alt text) provided alongside figures in this article has been generated by Frontiers with the support of artificial intelligence and reasonable efforts have been made to ensure accuracy, including review by the authors wherever possible. If you identify any issues, please contact us.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Footnotes

Edited by: Marco Dadda, University of Padua, Italy

Reviewed by: Guenther Witzany, Independent Researcher, Bürmoos,Austria