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Vision in Plants via Plant-Specific Ocelli?
Abstract
Although plants are sessile organisms, almost all of their organs move in space and thus require plant-specific senses to find their proper place with respect to their neighbours. Here we discuss recent studies suggesting that plants are able to sense shapes and colours via plant-specific ocelli.
... Plants perform neuronal-like computation not just for rapid and effective adaptation to an ever-changing physical environment but also for the sharing of information with other plants of the same species and for communication with bacteria and fungi [24,22,25,18,17,23,21,19,33]. In fact, plants emerge as social organisms. ...
... Root apexes are attracted to humidity [10] and a range of chemical compounds [32,37,19,6,33,38]. A root propagates towards the domain with highest concentration of attractants. ...
... The mathematical and engineering problems to be solved will be represented in plant root networks of resistive elements or reaction elements, involving capacitance and inductance as well as resistance, to model spatial distribution of voltage, current, electrical potential in space, temperature, pressure [88,66,106]. Implementations Our results can be also applied in fabrication of biosensors based on carbon nanotubes [16], molecular probing in single cells [17], dielectric spectroscopy [18], optical detection of plant physiological activity [19], modification of plant roots morphology [20], targeted delivery of nano particulate material to treat plant deceases [21,22] and stimulating plant growth [23]. ...
We discuss possible designs and prototypes of computing systems that could be based on morphological development of roots, interaction of roots, and analog electrical computation with plants, and plant-derived electronic components. In morphological plant processors data are represented by initial configuration of roots and configurations of sources of attractants and repellents; results of computation are represented by topology of the roots' network. Computation is implemented by the roots following gradients of attractants and repellents, as well as interacting with each other. Problems solvable by plant roots, in principle, include shortest-path, minimum spanning tree, Voronoi diagram, -shapes, convex subdivision of concave polygons. Electrical properties of plants can be modified by loading the plants with functional nanoparticles or coating parts of plants of conductive polymers. Thus, we are in position to make living variable resistors, capacitors, operational amplifiers, multipliers, potentiometers and fixed-function generators. The electrically modified plants can implement summation, integration with respect to time, inversion, multiplication, exponentiation, logarithm, division. Mathematical and engineering problems to be solved can be represented in plant root networks of resistive or reaction elements. Developments in plant-based computing architectures will trigger emergence of a unique community of biologists, electronic engineering and computer scientists working together to produce living electronic devices which future green computers will be made of.
... Or, to be more precise, plants do not need to have eyes: some authors may interpret that plants in fact 'see' due to their phytochrome-or cryptochrome-mediated perception of light intensity, orientation, and quality [9,11]. In his recent commentary [1] on our conceptual paper related to plant ocelli [2], Ernesto Gianoli expresses concerns about the plausibility of plant vision via plant-specific ocelli. Gianoli is critical of vision-like processes in plants in general, and of plant ocelli in particular. ...
... To mimic precisely complex objects such as leaves, Boquila must be capable of sensing parameters such as shape, dimension, and color [1,2,11]. In other words, it must be able to perceive vectorial sensory information. ...
... The most important among these viruses are begomoviruses (family Geminiviridae), although B. tabaci is also a vector of criniviruses, ipomoviruses, torradoviruses, and some carlaviruses. Begomoviruses are the most widespread plant viruses and cause devastating yield losses to many economically important crops, such as cotton, cassava, beans, tomato, and cucurbits [2]. Collectively, B. tabaci and begomoviruses are a major threat to global agriculture and food security. ...
In his recent commentary [1] on our conceptual paper related to plant ocelli [2], Ernesto Gianoli expresses concerns about the plausibility of plant vision via plant-specific ocelli. Gianoli is critical of vision-like processes in plants in general, and of plant ocelli in particular. Specifically, he highlights the processes potentially involved in leaf mimicry of the climbing plant Boquila trifoliolata, for which he prefers other explanations, such as volatile signaling and horizontal gene transfer on an ecological timescale [1].
... 32,33 Furthermore, it cannot be excluded that they may be able to discriminate detailed features of what surrounds them via a primitive visual system. 34 Evidence suggests that the leaf upper and sub-epidermis comprise cells suitable to act as ocelli, allowing plants to experience a sort of vision. 34,35 Support for this contention comes from studies on leaf mimicry in climbing plants 36 and photoreceptor-mediated kin recognition of Arabidopsis seedlings. ...
... 34 Evidence suggests that the leaf upper and sub-epidermis comprise cells suitable to act as ocelli, allowing plants to experience a sort of vision. 34,35 Support for this contention comes from studies on leaf mimicry in climbing plants 36 and photoreceptor-mediated kin recognition of Arabidopsis seedlings. 37 Both reports suggest plants can gather information about their environmental setting through visionbased inputs and behave accordingly. ...
Previous studies on the kinematics of pea plants' ascent and attach behavior have demonstrated that the signature of their movement varies depending on the kind of support. So far, these studies have been confined to artificial supports (e.g. wooden sticks). Little is known regarding the conditions under which pea plants could rely on biological supports (e.g. neighboring plants) for climbing toward the light. In this study, we capitalize on the 3D kinematic analysis of movement to ascertain whether pea plants scale their kinematics differently depending on whether they aim for artificial or biological support. Results suggest that biological support determines a smoother and more accurate behavior than that elicited by the artificial one. These results shed light on pea plants' ability to detect and classify the properties of objects and implement a movement plan attuned to the very nature of the support. We contend that such differences depend on the augmented multisensory experience elicited by the biological support.
... 20,21 According to Gottlieb Haberlandt's 22 hypothesis of plant ocelli, the upper epidermal cells of leaves are shaped like convex or Plano convex lenses. 23 By gathering light rays together, these "lenses" allow light-sensitive epidermal cells to recognize the size and shape of other plants in their surroundings. In addition to the leaves, the root apex may also have ocelli, since the roots can adapt to lower levels of light in the soil. ...
... 22 Haberlandt's theory was tested experimentally 42 as well as supported by studies of a mimicking plant Boquila trifoliolata. 23,43,44 This plant has the intriguing ability to change the shape of its leaves according to the host plant. When plastic leaves were presented to Boquila trifoliolata, it changed the shapes of leaves from three-lobed leaves to longitudinal leaves, mimicking the plastic leaves too. ...
Plants can activate protective and defense mechanisms under biotic and abiotic stresses. Their roots naturally grow in the soil, but when they encounter sunlight in the top-soil layers, they may move away from the light source to seek darkness. Here we investigate the skototropic behavior of roots, which promotes their fitness and survival. Glutamate-like receptors (GLRs) of plants play roles in sensing and responding to signals, but their role in root skototropism is not yet understood. Light-induced tropisms are known to be affected by auxin distribution, mainly determined by auxin efflux proteins (PIN proteins) at the root tip. However, the role of PIN proteins in root skototropism has not been investigated yet. To better understand root skototropism and its connection to the distance between roots and light, we established five distance settings between seedlings and darkness to investigate the variations in root bending tendencies. We compared differences in root skototropic behavior across different expression lines of Arabidopsis thaliana seedlings (atglr3.7 ko, AtGLR3.7 OE, and pin2 knockout) to comprehend their functions. Our research shows that as the distance between roots and darkness increases, the root’s positive skototropism noticeably weakens. Our findings highlight the involvement of GLR3.7 and PIN2 in root skototropism.
... But, how do the plants sense the thickness of the stimulus? Although we cannot single out one particular sensory mechanism to be involved in thickness sensing during circumnutation, plants have at their disposal an array of sensory modalities 42,43 including vision [44][45][46] , acoustic perception 47 , chemosensory perception 48,49 , all of which might be useful to this endeavour. Further, plant apexes are equipped with electrical, chemical, vibrational, gravitational and optical sensory transducers that permit the apex to sense the environment and provide the necessary information to plan a movement. ...
... First, we consider a visuomotor transformation in which the visual coding of the object's intrinsic properties (e.g., thickness) is transformed into a pattern of movement. Evidence suggests that the leaf upper and sub-epidermis comprise cells suitable to act as ocelli allowing plants to experience a sort of vision 45,46,50 . Support to this contention comes from studies on leaf mimicry in climbing plants 41 and photoreceptor-mediated kin recognition of Arabidopsis seedlings 44 . ...
Although plants are essentially sessile in nature, these organisms are very much in tune with their environment and are capable of a variety of movements. This may come as a surprise to many non-botanists, but not to Charles Darwin, who reported that plants do produce movements. Following Darwin’s specific interest on climbing plants, this paper will focus on the attachment mechanisms by the tendrils. We draw attention to an unsolved problem in available literature: whether during the approach phase the tendrils of climbing plants consider the structure of the support they intend to grasp and plan the movement accordingly ahead of time. Here we report the first empirical evidence that this might be the case. The three-dimensional (3D) kinematic analysis of a climbing plant (Pisum sativum L.) demonstrates that the plant not only perceives the support, but it scales the kinematics of tendrils’ aperture according to its thickness. When the same support is represented in two-dimensions (2D), and thus unclimbable, there is no evidence for such scaling. In these circumstances the tendrils’ kinematics resemble those observed for the condition in which no support was offered. We discuss these data in light of the evidence suggesting that plants are equipped with sensory mechanisms able to provide the necessary information to plan and control a movement.
... These cells were considered as plant ocelli, a type of simple eye common to invertebrates (Haberlandt 1905). Baluška and Mancuso (2016) proposed that focusing of light by these cells on plastoglobuli of epidermal amyloplasts and subepidermal chloroplasts can impart some form of vision capability. The recent reports on the behaviour of higher plants towards their kin or their host plants rekindled the concept of plants having a form of vision. ...
... As described earlier, Arabidopsis can recognise kin from non-kin by perceiving the plant shape of their neighbours presumably by monitoring the re ected light. While it is argued that such kin recognition and leaf mimicry may involve plant-speci c vision using plant ocelli (Baluška and Mancuso 2016), there are concerns about this possibility of plant vision (Gianoli 2017). However, Mancuso and Balu ka (2017) are of the opinion that as de ned by Nilsson and Daniel (2014) for bacteria, the behaviour or movement based on directional light perception can be regarded as vision. ...
In the late nineteenth century, Charles Darwin observed that ‘light exerts a powerful influence on most vegetable tissues, and there can be no doubt that it generally tends to check their growth’ (The Power of Movement in Plants, 1880). Subsequent to this seminal work, light has been recognised as an important regulator of plant growth. Over the next 150 years, research on light regulation of plant growth and development by immensely imaginative and talented researchers in various laboratories across the globe has given us tremendous insights into how light governs plant growth both at the organismal and molecular levels. The discovery of light-responsive photoreceptor proteins that are activated by red, far-red, blue/UV-A and UV-B light has helped further our understanding of how plants respond to the light that falls on the surface of the earth. This chapter brings together the recent developments in our understanding of how plants sense light by using photoreceptors and the various molecular mechanisms involved in light perception and transmission of the light signal within the plant. Furthermore, the chapter discusses recently ascribed functions of photoreceptors such as the ability of plants to distinguish their kin from non-kin through the action of phytochrome, the role(s) of cryptochrome as a magnetoreceptor and the role of phytochrome and phototropin as temperature sensors. The chapter also rekindles the debate about whether plants can have vision despite the lack of optical or light-sensitive organs such as eyes.
... Gottlieb Haberlandt was the first to propose this idea back in 1905, with it gaining further support from Charles Darwin and Harold Wager. In the first quarter of the 21st century, S. Mancuso further developed the plant "vision" hypothesis (Baluška and Mancuso, 2016). By interacting with the Plantoverse and trying out non-human optics, we are not only able to look at the other as a subject of its own life but to also reconsider the boundaries of relationships within a multispecies ecosystem. ...
Humans constantly interact with their environment, with other humans, as well as natural and artificial non-human agents. Nevertheless, our somatosensory system limits the diversity of our ways of communicating. Such organisms as plants thus escape our notice, blending into the landscape. This phenomenon is called Plant blindness. This leads not only to indifference and lack of empathy towards plants among ordinary people but also to a deficit in funding plant conservation. We believe that it is important to develop connections and also rethink the relationship between humans and flora. This paper examines the Plant turn in the context of an art-science project titled Plantoverse. The scientific part of the project is based on a study of plant epidermis cells, which possess optical properties and function as a “lens”. The data acquired via confocal microscopy was used to construct a mathematical model of these lenses which in turn formed the basis of the artistic work. It is a representation of the plant epidermis in a digital environment. The work allows us to look at ourselves through “plant optics'' and find new tools for interacting with the vegetal world. This interdisciplinary approach can help transfer knowledge about flora from the professional environment to lay society and form a new, more empathetic view toward plants.
... Such ability to integrate signals is also demonstrated at the tissue level when collective stomatal behavior changes under different external cues (light and drought), affecting photosynthetic efficiencies-as showed in the mathematical simulations by Sukhova et al. [5]. Exemplifying the plethora of sophisticated mechanisms used by plants to sense their environment, Yamashita and Baluska [6] propose that plant eye-like ocelli, which allow plant-specific kind of vision [7,8] and which evolved from the algal ocelloids, are part of complex plant sensory systems and guide cognition-based plant behavior, such as the mimicking of diverse host plants by woody vine Boquila trifoliata [9][10][11] and root light escape tropism [12]. ...
Being sessile organisms that need to effectively explore space (above and below ground) and acquire resources through growth, plants must simultaneously consider multiple possibilities and wisely balance the energy they spend on growth with the benefits for survival [...]
... The Haberlandt plant ocelli theory is not surprising if we consider that various organisms such as bacteria, algae, and fungi (as discussed below) have cells with similar light-sensing properties. However, plant ocelli theory was almost forgotten and only recently revived [8,9]. Supporting this leaf epidermal ocelli scenario, leaf epidermis cells, with the exception of stomata guard cells, do not generate photosynthetic chloroplasts, although they have the best position with respect to the amount of light they receive. ...
Vision is essential for most organisms, and it is highly variable across kingdoms and domains of life. The most known and understood form is animal and human vision based on eyes. Besides the wide diversity of animal eyes, some animals such as cuttlefish and cephalopods enjoy so-called dermal or skin vision. The most simple and ancient organ of vision is the cell itself and this rudimentary vision evolved in cyanobacteria. More complex are so-called ocelloids of dinoflagellates which are composed of endocellular organelles, acting as lens- and cornea/retina-like components. Although plants have almost never been included into the recent discussions on organismal vision, their plant-specific ocelli had already been proposed by Gottlieb Haberlandt already in 1905. Here, we discuss plant ocelli and their roles in plant-specific vision, both in the shoots and roots of plants. In contrast to leaf epidermis ocelli, which are distributed throughout leaf surface, the root apex ocelli are located at the root apex transition zone and serve the light-guided root navigation. We propose that the plant ocelli evolved from the algal ocelloids, are part of complex plant sensory systems and guide cognition-based plant behavior.
... Morphological and functional resemblances between plant leaves, the human brain, plant roots, and the human gut were suggested [247,248]. In addition, the similarities between quantum phenomena occurring during photosynthesis and consciousness in the brain have been described [249]. Light and food are factors that play roles in both plants and humans, implying that the root-leaf axis is the evolutionary ancestor of the gut-brain axis. ...
Variability characterizes the complexity of biological systems and is essential for their function. Microtubules (MTs) play a role in structural integrity, cell motility, material transport, and force generation during mitosis, and dynamic instability exemplifies the variability in the proper function of MTs. MTs are a platform for energy transfer in cells. The dynamic instability of MTs manifests itself by the coexistence of growth and shortening, or polymerization and depolymerization. It results from a balance between attractive and repulsive forces between tubulin dimers. The paper reviews the current data on MTs and their potential roles as energy-transfer cellular structures and presents how variability can improve the function of biological systems in an individualized manner. The paper presents the option for targeting MTs to trigger dynamic improvement in cell plasticity, regulate energy transfer, and possibly control quantum effects in biological systems. The described system quantifies MT-dependent variability patterns combined with additional personalized signatures to improve organ function in a subject-tailored manner. The platform can regulate the use of MT-targeting drugs to improve the response to chronic therapies. Ongoing trials test the effects of this platform on various disorders.
... For example, it has been advanced that proprioception may allow climbing plants to perceive the position of their tendrils, which provides the feedback information necessary for adjusting their aperture to the thickness of the support [27,28]. In addition, plants may have at their disposal some systems typically involved in the reception of light and the capacity to build a representation of the surrounding environment [29,30]. Continuing this analysis, recent studies report that plants may get information about their surroundings by emitting sonic clicks (i.e., clicking) and perceiving the returning echoes [31]. ...
Plants such as climbers characterized by stems or tendrils need to find a potential support (e.g., pole, stick, other plants or trees) to reach greater light exposure. Since the time when Darwin carried out research on climbing plants, several studies on plants’ searching and attachment behaviors have demonstrated their unique ability to process some features of a support to modulate their movements accordingly. Nevertheless, the strategies underlying this ability have yet to be uncovered. The present research tries to fill this gap by investigating how the interaction between above- (i.e., stems, tendrils, …) and below-ground (i.e., the root system) plant organs influences the kinematics of their approach-to-grasp movements. Using three-dimensional (3D) kinematic analysis, we characterized the movements of pea plants (Pisum sativum L.) as they leaned towards supports whose below- and above-ground parts were characterized by different thicknesses (i.e., thin below- thick above-ground, or the opposite). As a control condition, the plants were placed next to supports with the same thickness below and above ground (i.e., either entirely thin or thick). The results suggest that the information regarding below- and above-ground parts of a support appears to be integrated and modulates the reach-to-grasp behavior of the plant. Information about the support conveyed by the root system seems to be particularly important to achieve the end-goal of movement.
... Nonetheless, to our knowledge, there is no documented evidence of changes in leaf shape elicited by volatiles and, more importantly, known volatilemediated responses in receiver plants are rather general [18][19][20][21] , while leaf mimicry in Boquila is highly specific. The second hypothesis, the horizontal gene transfer (HGT) hypothesis, has been deemed implausible [22][23][24] . However, evidence from other study systems suggests that the HGT hypothesis is not too speculative. ...
The mechanisms behind the unique capacity of the vine Boquila trifoliolata to mimic the leaves of several tree species remain unknown. A hypothesis in the original leaf mimicry report considered that microbial vectors from trees could carry genes or epigenetic factors that would alter the expression of leaf traits in Boquila. Here we evaluated whether leaf endophytic bacterial communities are associated with the mimicry pattern. Using 16S rRNA gene sequencing, we compared the endophytic bacterial communities in three groups of leaves collected in a temperate rainforest: (1) leaves from the model tree Rhaphithamnus spinosus (RS), (2) Boquila leaves mimicking the tree leaves (BR), and (3) Boquila leaves from the same individual vine but not mimicking the tree leaves (BT). We hypothesized that bacterial communities would be more similar in the BR–RS comparison than in the BT–RS comparison. We found significant differences in the endophytic bacterial communities among the three groups, verifying the hypothesis. Whereas non-mimetic Boquila leaves and tree leaves (BT–RS) showed clearly different bacterial communities, mimetic Boquila leaves and tree leaves (BR–RS) showed an overlap concerning their bacterial communities. The role of bacteria in this unique case of leaf mimicry should be studied further.
... For example, it has been advanced that proprioception may allow climbing plants to perceive the position of their tendrils, which provides the feedback information necessary for adjusting their aperture to the thickness of the support [27,28]. In addition, plants may have at their disposal some systems typically involved in the reception of light and the capacity to build a representation of the surrounding environment [29,30]. Continuing this analysis, recent studies report that plants may get information about their surroundings by emitting sonic clicks (i.e., clicking) and perceiving the returning echoes [31]. ...
Plants characterized by a soft or weak steam, such as climbing plants, need to find a potential support (e.g., wooden trunk) to reach greater light exposure. Since Darwin’s research on climbing plants, several studies on their searching and attachment behaviors have demonstrated their unique ability to process different support features to modulate their movements accordingly. Nevertheless, the strategies underlying this ability are yet to be uncovered. The present research tries to fill this gap by investigating how the interaction between above- (i.e., stem, tendril, …) and belowground (i.e., the root system) plant organs influence the kinematics of the approach-to-grasp movement. With three-dimensional (3D) kinematical analysis, we characterized the movement of pea plants (Pisum sativum L.) towards a support with different thicknesses above and belowground (i.e., thin below, thick aboveground, or the opposite). As a control condition, the plants were presented to supports with the same thickness below- and aboveground (i.e., either entirely thin or thick). The results suggest an integration between the information from below- and aboveground for driving the reach-to-grasp behavior of the aerial plant organs. Information about the support conveyed by the root system seems particularly important to fulfil the end-goal of the movement.
... In line with previous research, two alternative hypotheses are VOCs airborne communication and horizontal gene transfer (Gianoli & Carrasco-Urra, 2014). However, taking into account that physical contact is not needed for mimicry to take place, a more radical hypothesis has been recently advanced: a plant-specific form of proto-vision akin to the ocelloidbased type of vision found in cyanobacteria and some dinoflagellates (Baluška & Mancuso, 2016. According to Baluška and Mancuso, the vine may be able to perceive shapes and colors via somewhat primitive image-forming mechanism (although see Gianoli, 2017). ...
Unlike animal behavior, behavior in plants is traditionally assumed to be completely determined either genetically or environmentally. Under this assumption, plants are usually considered to be noncognitive organisms. This view nonetheless clashes with a growing body of empirical research that shows that many sophisticated cognitive capabilities traditionally assumed to be exclusive to animals are exhibited by plants too. Yet, if plants can be considered cognitive, even in a minimal sense, can they also be considered conscious? Some authors defend that the quest for plant consciousness is worth pursuing, under the premise that sentience can play a role in facilitating plant's sophisticated behavior. The goal of this article is not to provide a positive argument for plant cognition and consciousness, but to invite a constructive, empirically informed debate about it. After reviewing the empirical literature concerning plant cognition, we introduce the reader to the emerging field of plant neurobiology. Research on plant electrical and chemical signaling can help shed light into the biological bases for plant sentience. To conclude, we shall present a series of approaches to scientifically investigate plant consciousness. In sum, we invite the reader to consider the idea that if consciousness boils down to some form of biological adaptation, we should not exclude a priori the possibility that plants have evolved their own phenomenal experience of the world.
This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition
Philosophy > Consciousness
Neuroscience > Cognition
... This third hypothesis would support the possibility that plant vision based on plant ocelli 4,5 is behind this unique form of plant behavior. 6,7 The plant ocelli concept was elaborated by Gottlieb Haberlandt in 1905 and two years later supported by Francis Darwin 8 which consists of the upper epidermis cells have a planoconvex or convex shape acting as lenses, allowing the convergence of light radiation into light-sensitive subepidermal cells. 5 With the discovery that the B. trifoliolata is able to mimic the leaves of the nearest plant, 1,3 we have been given a rare opportunity to test plant vision in more detail. ...
Upon discovery that the Boquila trifoliolata is capable of flexible leaf mimicry, the question of the mechanism behind this ability has been unanswered. Here, we demonstrate that plant vision possibly via plant-specific ocelli is a plausible hypothesis. A simple experiment by placing an artificial vine model above the living plants has shown that these will attempt to mimic the artificial leaves. The experiment has been carried out with multiple plants, and each plant has shown attempts at mimicry. It was observed that mimic leaves showed altered leaf areas, perimeters, lengths, and widths compared to non-mimic leaves. We have calculated four morphometrical features and observed that mimic leaves showed higher aspect ratio and lower rectangularity and form factor compared to non-mimic leaves. In addition, we have observed differences in the leaf venation patterns, with the mimic leaves having less dense vascular networks, thinner vascular strands, and lower numbers of free-ending veinlets.
... To begin with, climbing plants seem to have evolved a plant-specific vision system that processes the intrinsic and extrinsic proprieties of the stimulus. The findings of several studies suggest that the upper and subepidermis parts of a leaf comprise cells acting as ocelli, eye-like structures, allowing plants to gather visual information about their environment (Baluška & Mancuso, 2016). Support for this concept has been produced by studies investigating Boquilla trifoliolata (Carrasco-Urra & Gianoli, 2009), which modifies the appearance of its leaves according to the host plant and perfectly mimics the colors, shapes, sizes, orientations, and petiole lengths of the leaves. ...
Tendrils are clasping structures used by climbing plants to anchor and support their vines that coil around suitable hosts to achieve the greatest exposure to sunlight. Although recent evidence suggests that climbing plants are able to sense the presence of a potential stimulus in the environment and to plan the tendrils' movements depending on properties such as its thickness, the mechanisms underlying thickness sensing in climbing plants have yet to be uncovered. The current research set out to use three-dimensional kinematical analysis to investigate if and in what way the root system contributed to thickness sensing. Experiment 1 was designed to confirm that the movement of the tendrils of pea plants (Pisum sativum L.) is planned and controlled on the basis of stimulus thickness when the stimulus is inserted into the substrate. Experiment 2 was designed to investigate what happens when the stimulus is lifted to the ground so as to impede the root system from sensing it. The results confirmed that tendrils' kinematics depend on thickness when the stimulus is available to the root system but not when it is unavailable to it. These findings suggest that the root system plays a pivotal role in sensing the presence and the thickness of a stimulus and that the information perceived affects the planning and the execution of the climbing plants' reach-to-grasp movements. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
... • The cells of plants did not evolve complex eyes, even though they are so dependent on sunlight. They are however suspected to have primitive vision-like capabilities [65]. 7) Senescence and death : Aging is attributed to factors like an unstable genome, exhaustion of stem cells, malfunction of mitochondria, etcetera [66], resulting in death of an organism. ...
The design of any artificial intelligence is an interdisciplinary pursuit that requires keeping within perspective, the various properties of matter and life in the known universe, while remaining cautious of biases and misconceptions that arise from the limitations of prior learning, available tools and sensory capabilities. This paper curates a vast collection of human knowledge gathered during the process of exploring and questioning the fundamentals of why the mechanisms that constitute life were built in specific ways, and re-questioning those facts using anomalies that sometimes contradict or expose errors in human assumptions of life and intelligence. A meta-analysis of such knowledge at a single glance also helps identify interesting patterns in various phenomena that can in-time, spur creative solutions, alter the direction of research, assist with intelligent inferences and hopefully result in the identification and creation of artificial intelligence.<br
... It is suggested that we can strike off the chance that the plant-host plant mimicry is VOC-mediated, as researchers in 2016 said: they made the claim that Boquila possesses the sense of sight, this being the least thrifty explanation for this complex phenomenon. 8 Instead, one clear evidence of a VOC-mediated response is the scent-perception that the Dodder plant displays. It was demonstrated that the parasitic plant Cuscuta pentagona (dodder) uses volatile cues for host location. ...
In a very recent book called Sensory Biology of Plants, published by renowned publisher Springer Nature, the authors stated that the scientific literature gathered so far regarding knowledge around the field of Plant Acoustics allows us to divert the focus from the question “whether plants perceive sound” toward the questions “how and why they are doing it” Some phenomena are well known: roots perceive the sound of flowing water and display a sound-mediated growth toward the water source, while the buzz pollination process allows plants to minimize the pollen lost and maximize which is collected by true pollinators. But plants are far more perceptive and responsive to their environment than we generally consider them to be, and they are communicating far more information than we realize if we only took all their signals (VOCs, sound, exudates, etc.) into a greater picture. Could Volatile Organic Compounds (VOCs) be involved in mediating more responses than we imagine? VOC synthesis and release is known to be elicited also by electrical signals caused by mechanical stimuli, touching and wounding being among these, serving as info-chemicals in the communication between plants (“eavesdropping”), and within the organs of the same plant, in order for it to get synchronized with its surroundings. This paper is an overview of the discoveries around plant perception with a focus on the link between mechanical stimuli, as sound vibrations are, and changes in plant physiology leading to VOC emission.
... Light cues are recognised as important for dodder foraging (Orr et al., 1996;Benvenuti et al., 2005;Wu et al., 2019). Additionally, in recent years, Haberlandt's plant ocelli hypothesis has been revisited with new pieces of evidence (Haberlandt, 1905;Baluška and Mancuso, 2016;Mancuso and Baluška, 2017). Parasitic plants rely on its senses for detecting hosts, and perhaps vision or some analogue sense could be of use. ...
In our study, we investigated some physiological and ecological aspects of the life of Cuscuta racemosa Mart. (Convolvulaceae) plants with the hypothesis that they recognise different hosts at a distance from them, and they change their survival strategy depending on what they detect. We also hypothesised that, as an attempt of prolonging their survival through photosynthesis, the synthesis of chlorophylls (a phenomenon not completely explained in these parasitic plants) would be increased if the plants don’t detect a host. We quantified the pigments related to photosynthesis in different treatments and employed techniques such as electrophysiological time series recording, analyses of the complexity of the obtained signals, and machine learning classification to test our hypotheses. The results demonstrate that the absence of a host increases the amounts of chlorophyll a, chlorophyll b, and β-carotene in these plants, and the content varied depending on the host presented. Besides, the electrical signalling of dodders changes according to the species of host perceived in patterns detectable by machine learning techniques, suggesting that they recognise from a distance different host species. Our results indicate that electrical signalling might underpin important processes such as foraging in plants. Finally, we found evidence for a likely process of attention in the dodders toward the host plants. This is probably to be the first empirical evidence for attention in plants and has important implications on plant cognition studies.
... For example, the woody vine Boquila trifoliata, from the rainforest of South America, is capable of mimicking shapes, size, colours and texture of up to three different host plants [128]. We have proposed that the ocelli concept of Gottlieb Haberlandt would be applicable here as it is almost impossible to explain mimicking of so many parameters without some kind of vision [129,130]. It should be not so surprising to have vision-supporting ocelli in vascular plants as eye-like ocelloids are involved in rudimentary vision of unicellular algae [131,132]. ...
Vascular plants are integrated into coherent bodies via plant-specific synaptic adhesion domains, action potentials (APs) and other means of long-distance signalling running throughout the plant bodies. Plant-specific synapses and APs are proposed to allow plants to generate their self identities having unique ways of sensing and acting as agents with their own goals guiding their future activities. Plants move their organs with a purpose and with obvious awareness of their surroundings and require APs to perform and control these movements. Self-identities allow vascular plants to act as individuals enjoying sociality via their self/non-self-recognition and kin recognition. Flowering plants emerge as cognitive and intelligent organisms when the major strategy is to attract and control their animal pollinators as well as seed dispersers by providing them with food enriched with nutritive and manipulative/addictive compounds. Their goal in interactions with animals is manipulation for reproduction, dispersal and defence.
This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens’.
... As early as 1905, Gottlieb Haberlandt suggested that the leaf upper and sub-epidermis comprise cells acting as ocelli, eye-like structures allowing plants to gather visual information about their environment [33]. Support to this contention comes from studies on Boquilla trifoliolata, a climbing wood vine, which modifies its leaves with perfect mimicking of the host plant leaves, even without a direct contact with it [34]. Coherently, plants may correct the trajectory of their tendril using visual information. ...
At first glance, plants seem relatively immobile and, unlike animals, unable to interact with the surroundings or escape stressful environments. But, although markedly different from those of animals, movement pervades all aspects of plant behaviour. Here, we focused our investigation on the approaching movement of climbing plants, that is the movement they perform to reach-to-climb a support. In particular, we examined whether climbing plants evolved a motor accuracy mechanism as to improve the precision of their movement and how this eventually differs from animal species. For this purpose, by means of three-dimensional kinematical analysis, we investigated whether climbing plants have the ability to correct online their movement by means of secondary submovements, and if their frequency production is influenced by the difficulty of the task. Results showed, not only that plants correct their movement in flight, but also that they strategically increase the production of secondary submovements when the task requires more precision, exactly as humans do. These findings support the hypothesis that the movement of plants is far cry from being a simple cause-effect mechanism, but rather is appropriately planned, controlled and eventually corrected.
... Moreover, the presence of more pollinating animals increases variability in the movements of the stamen. In other words, it seems that the plants are able to perceive, 'see' (Baluska & Mancuso, 2016) and 'hear' (Zaraska, 2017). In particular, the plants developed a selective bond with pollinating animals. ...
Plants are not just passive living beings that exist in nature. They are complex and highly adaptable species that react sensitively to environmental forces/stimuli with movement, morphological changes and through the communication of volatile molecules. In a way, plants mimic some traits of animal and human behavior; they compete for limited resources by gaining more area for more sunlight and spreading their roots underground. Furthermore, in order to survive and thrive, they evolve and “learn” to control various environmental stress factors in order to increase the yield of flowering, fertilization and germination processes. The concept of associating complex behavior, such as intelligence, with plants is still a highly debatable topic among researchers worldwide. Recent studies have shown that plants are able to discriminate between positive and negative experiences and “learn” from them. Some botanists have interpreted these behavioral data as a form of primordial cognitive processes. Others have evaluated these responses as biological automatisms of plants determined by adaptation to the environment and absence of intelligence. This review aimed to explore adaptive behavioral aspects of various plant species distributed in different ecosystems by emphasizing their biological complexity and survival instinct.
... This bio sonar may provide information about the thickness of the support to the plants, which will act accordingly. Second, several studies have suggested that the leaf's upper and subepidermis comprise cells acting as ocelli, eye-like structures allowing plants to gather visual information about their environment (Baluška & Mancuso, 2016). Support for this contention comes from studies on Boquilla trifoliolata, a climbing wood vine that modifies the appearance of its leaves according to the host plant, perfectly mimicking the colors, shapes, sizes, orientations, and petiole lengths of the leaves. ...
Speed–accuracy trade-off (SAT) is the tendency for decision speed to covary with decision accuracy. SAT is an inescapable property of aimed movements being present in a wide range of species, from insects to primates. An aspect that remains unsolved is whether SAT extends to plants’ movement. Here, we tested this possibility by examining the swaying in circles of the tips of shoots exhibited by climbing plants (Pisum sativum L.) as they approach to grasp a potential support. In particular, by means of three-dimensional kinematical analysis, we investigated whether climbing plants scale movement velocity as a function of the difficulty to coil a support. Results showed that plants are able to process the properties of the support before contact and, similarly to animal species, strategically modulate movement velocity according to task difficulty.
... Leaf epidermal ocelli can focus light onto the epidermal basal membrane that can sense changing light patterns and thus act as a sensory epithelium (Baluška and Mancuso 2016;Gianoli 2016;Haberlandt, 1914. p. 626). ...
... Leaf epidermal ocelli can focus light onto the epidermal basal membrane that can sense changing light patterns and thus act as a sensory epithelium (Baluška and Mancuso 2016;Gianoli 2016;Haberlandt, 1914. p. 626). ...
Hypotheses:
The drive to survive is a biological universal. Intelligent behaviour is usually recognised when individual organisms including plants, in the face of fiercely competitive or adverse, real world circumstances, change their behaviour to improve their probability of survival.
Scope:
This article explains the potential relationship of intelligence to adaptability and emphasises the need for recognising individual variation in intelligence showing it to be goal directed and thus being purposeful. Intelligent behaviour in single cells and microbes is frequently reported. Individual variation might be underpinned by a novel learning mechanism described in detail. The requirements for real world circumstances are outlined, the relationship to organic selection indicated together with niche construction as a good example of intentional behaviour that should improve survival. Adaptability is important in crop development but the term may be complex incorporating numerous behavioural traits some of which are indicated.
Conclusion:
There is real biological benefit to regarding plants as intelligent both from a fundamental issue of understanding plant life but also from providing a direction for fundamental future research and in crop breeding.
... 14 In this respect, recent research has made progress by showing that "detection" is possiblebesides a mechanic triggering as in nectar scales of Loasaceae 15even through visual and acoustic sensing. 16,17 The latter study moreover reports that the plant in response to bee sounds "adjust their reproductive characteristics" by initiating nectar secretion. Loasaceae flowers in addition possess the ability of a quick stamen movement (only few minutes 18 ), and to remember previous visitation patterns (as shown in this study), fulfilling the requirements of intelligent plant behavior. ...
Plants – and their pollinating counterparts – display complex and sophisticated mechanisms to achieve successful pollination. It probably was only a matter of time for proof of plant intelligence in the context of floral ecology to surface, i.e. the memorization of previous events and a corresponding adjustment of flower behavior. In a recent study we presented a large experimental dataset on the evolution of stamen movement patterns observed in Loasaceae and the apparent role of plant behavior in the diversification of this plant group. The findings at species level suggest that individual plants may be able to adjust the timing of their pollen presentation to the actual pollination scenario they experience. Here we provide first evidence for a pre-emptive stamen presentation in Nasa poissoniana (Loasaceae), based on previously experienced pollinator visitation intervals. Using the unique ability of fast and precise stamen movements in response to a previous stimulus of the nectar scales, the plants should be able to reduce pollen loss and increase outbreeding success via optimizing the timing of male function. We discuss this behavior and its implications in the light of the recent literature and propose questions for future investigations.
... Although plants are sessile organisms, almost all of their organs move in space and thus require plant-specific senses to find their proper place with respect to their neighbours. Recent studies have suggested that plants are able to sense shapes and colours via plant-specific ocelli ( Baluška and Mancuso, 2016). Light plays a major signaling role in plant development is not surprising. ...
Intelligence is the ability to solve problems and plants are amazingly good in solving their problems. Each choice a plant makes is based on a type of mathematical calculation. The bottom of the plant may be the most sophisticated of all though. Plants are complex communicators and communicate in a wide variety of ways. They use chemical volatiles, electrical signals and even vibrations. The strength of this evolutionary choice is that it allows a plant to survive even after losing ninety percent or more of its biomass. Plants are built of a huge number of basic modules that interact as nodes of a network. Plants have evolved an incredible variety of toxic compounds to ward off predators. When attacked by an insect, many plants release a specific chemical compound. If plants can do all these then they must be intelligent. Recent advances in plant molecular biology, cellular biology, electrophysiology and ecology, unmask plants as sensory and communicative organisms, characterized by active, problem solving behavior. Unfortunately scientists have not yet discovered any brain or neuronal network in plants. It is said that the reactions within signaling pathways may provide a biochemical basis for learning and memory in addition to computation and problem solving. One of most enigmatic and astounding characters of plants, especially trees is the ascent of sap or upward movement of water through stem, which is up to 300 ft in height. The water moves up to this height from the roots which are spread very deep in the soil. Amazingly, it largely occurs by a passive process called transpiration pull. We have made so much advancement in science and technology but we are unfortunately cannot emulate this feet of plants. This paper is a compilation of observations, experiments and studies made to understand the amazing and unresolved aspects of intelligence in plants.
... Light may blocked or its intensity reduced depending upon the distribution and density of organic and inorganic materials surrounding a given plant. Recently, it has been convincingly and realistically hypothesized that plants could have developed a form of primitive vision ability allowing them to receive and process large amounts of information provided by light [4,5]. Furthermore, light interaction with auxin, elicits local responses as well as long-distance signalling. ...
Living organisms tend to find viable strategies under ambient conditions that optimize their search for, and utilization of, life-sustaining resources. For plants, a leading role in this process is performed by auxin, a plant hormone that drives morphological development, dynamics, and movement to optimize the absorption of light (through branches and leaves) and chemical "food" (through roots). Similarly to auxin in plants, serotonin seems to play an important role in higher animals, especially humans. Here, it is proposed that morphological and functional similarities between (i) plant leaves and the animal/human brain and (ii) plant roots and the animal/human gastro-intestinal tract have general features in common. Plants interact with light and use it for biological energy, whereas, neurons in the central nervous system seem to interact with biophotons and use them for proper brain function. Further, as auxin drives the "arborescence" of roots within the soil, similarly serotonin seems to facilitate enteric nervous system connectivity within the human gastrointestinal tract. This auxin/serotonin parallel suggests the root- branch axis in plants may be an evolutionary precursor to the gastrointestinal-brain axis in humans. Finally, it is hypothesized that light might be an important factor, both in gastrointestinal dynamics and brain function. Such a comparison may indicate a key role for the interaction of light and serotonin in neuronal physiology (possibly in both the central nervous system and the enteric nervous system), and according to recent work, mind and consciousness.
... But the possibility of machine sentience might strike behavioral neuroscientists, maybe Woodruff included, as too much of a stretch. They, like many others, might find functionalism too permissive and thus react similarly to another hypothesis, likewise possible under functionalism: plant sentience (Baluška & Mancuso, 2016;Smith, 2016, Ch. 2). Still, the possibility of plant sentience, too, makes the hypothesis of fish sentience entirely unsurprising, which makes Woodruff's case seem less radical. ...
Woodruff's case for fish sentience is intriguing. Though far from ready for final acceptance, it is worth pursuing. The case is philosophically uncontroversial under functionalism and reductive materialism. It is also highly heuristic, as it raises interesting issues for further investigation, such as the neural causation of behavior, the role of Mauthner cells in conditioned avoidance, and whether operant conditioning is constitutive of fish sentience. Professor in the Center for Behavioral Studies and Investigations, University of Guadalajara, does research on neural network modelling of learning and philosophy of psychology. He is editor of Behavior and Philosophy. www.ceic.cucba.udg.mx/Investigacion/personal-investigador?id=4 Woodruff (2017) makes a case for the hypothesis (a term he repeatedly uses, to the benefit of his case) that certain fish (the Actinopterygii class, which includes the Teleostei infraclass and forms over 90% of living fish) could have phenomenal consciousness (subjective qualitative experiences), or "sentience" for short. Woodruff joins forces with others he cites to reject the claim that fish lack sentience. This negative claim has been made on two grounds. (1) Fish lack the kind of complex neuroanatomical organization presumably "necessary" (more on this seemingly innocent word below) for sentience (viz., a layered neocortex that receives substantial projections from the thalamus, or something near enough or "homologous"). (2) Fish also lack the kinds of complex behaviors often linked to sentience. Against both (1) and (2), Woodruff reviews evidence that fish have neuroanatomical structures (optic tectum, pallium) with the required organization, physiology, and sensory and behavioral correlates (e.g., conditioned avoidance) to meet the requirements for at least one kind of sentience, namely, visual phenomenal consciousness. I find Woodruff's case scientifically intriguing-at least no less so than other cases of evidential support for hypotheses in science. He follows the tried-and-true scientific strategy of mustering as much evidential support as available for a tentative, preliminary, suggestive, but scientifically educated supposition. The evidence he presents strikes me as clear and diverse enough to treat the hypothesis at least as worthy of further scientific inquiry. I missed a discussion of Mauthner (M) cells (a pair of readily identifiable reticulospinal neurons in the hindbrain near the entry of cranial nerve VIII, just under the fourth ventricle in teleosts and some amphibians), as they are a much-investigated neural substrate of the
... been convincingly and realistically hypothesized that plants could have developed a form of primitive vision ability allowing them to receive and process a large amount of information provided by light (Baluška and Mancuso [3]; Mancuso and Baluška [33]). Furthermore, light interacting with auxin, elicits local responses as well as long-distance signaling. ...
Living organisms tend to find viable strategies under ambient conditions that optimize their search for, and utilization of, life-sustaining resources. For plants, a leading role in this process is performed by auxin, a plant hormone that drives morphological development, dynamics, and movement to optimize the absorption of light (through branches and leaves) and chemical "food" (through roots). Similarly to auxin in plants, serotonin seems to play an important role in higher animals, especially humans. Here, it is proposed that morphological and functional similarities between (i) plant leaves and the animal/human brain and (ii) plant roots and the animal/human gastro-intestinal tract have general features in common. Plants interact with light and use it for biological energy, whereas, neurons in the central nervous system seem to interact with bio-photons and use them for proper brain function. Further, as auxin drives roots "arborescence" within the soil, similarly serotonin seems to facilitate enteric nervous system connectivity within the human gastro-intestinal tract. This auxin/serotonin parallel suggests the root-branches axis in plants may be an evolutionary precursor to the gastro-intestinal-brain axis in humans. Finally, we hypothesize that light might be an important factor, both in gastro-intestinal dynamics and brain function. Such a comparison may indicate a key role for the interaction of light and serotonin in neuronal physiology (possibly in both the central nervous system and the enteric nervous system), and according to recent work, mind and consciousness.
... Again the sensing requires receptors able to discriminate the particular group of VOCs. However, Mancuso & Baluska [138] have creatively suggested that plants do possess primitive eyes, that is ocelli, based on a very early suggestion by Haberlandt. These might provide the necessary discrimination [139]. ...
Intelligence is defined for wild plants and its role in fitness identified. Intelligent behaviour exhibited by single cells and systems similarity between the interactome and connectome indicates neural systems are not necessary for intelligent capabilities. Plants sense and respond to many environmental signals that are assessed to competitively optimize acquisition of patchily distributed resources. Situations of choice engender motivational states in goal-directed plant behaviour; consequent intelligent decisions enable efficient gain of energy over expenditure. Comparison of swarm intelligence and plant behaviour indicates the origins of plant intelligence lie in complex communication and is exemplified by cambial control of branch function. Error correction in behaviours indicates both awareness and intention as does the ability to count to five. Volatile organic compounds are used as signals in numerous plant interactions. Being complex in composition and often species and individual specific, they may represent the plant language and account for self and alien recognition between individual plants. Game theory has been used to understand competitive and cooperative interactions between plants and microbes. Some unexpected cooperative behaviour between individuals and potential aliens has emerged. Behaviour profiting from experience, another simple definition of intelligence, requires both learning and memory and is indicated in the priming of herbivory, disease and abiotic stresses. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
... The roots grow inside the channels. The roots apexes navigate along the channel using mechanical, acoustic (Gagliano et al., 2012) and visual (Mo et al., 2017;Baluška and Mancuso, 2016) means. Root apexes exhibit a positive gravitropism (Darwin et al., 1899;Pfeffer, 1894;Baluška et al., 1996;Baluška and Hasenstein, 1997;Masi et al., 2008). ...
Theoretical constructs of logical gates implemented with plant roots are morphological computing asynchronous devices. Values of Boolean variables are represented by plant roots. A presence of a plant root at a given site symbolises the logical {\sc True}, an absence the logical {\sc False}. Logical functions are calculated via interaction between roots. Two types of two-inputs-two-outputs gates are proposed: a gate where root apexes are guided by gravity and a gate where root apexes are guided by humidity. We propose a design of binary half-adder based on the gates.
This chapter focuses on a single but essential building block of biological organisation, namely the way living organisms establish their specific relationship between existence and appearance. Although in the following we restrict our interest to the visual dimension, one could conceive of other modalities and their interactions along similar lines. All lineages which led to complex multicellularity have either one or both of the following advanced light-handling skills: (i) light reflection and absorption to create a display of self and/or (ii) the ability to focus the light reflected from other objects on a pigmented retina so as to create an image of the external world. Inanimate objects also reflect light, but only living entities can actively influence their reflection and therefore also their display. Living bodies themselves create the exposed surfaces. Such appearances are therefore in effect an externalisation of an organised self – and that is something that does not apply to the visual aspects of inanimate things. Further, I argue that the organismal capacity of self-representation is intimately related to certain essential characteristics which differentiate life from nonlife. The more developed the self-representational ability, the higher the complexity of organisation, and the further away the organised beings are from nonlife.
The 21st-century “plant neurobiology” movement is an amalgam of scholars interested in how “neural processes”, broadly defined, lead to changes in plant behavior. Integral to the movement (now called plant behavioral biology) is a triad of historically marginalized subdisciplines, namely plant ethology, whole plant electrophysiology and plant comparative psychology, that set plant neurobiology apart from the mainstream. A central tenet held by these “triad disciplines” is that plants are exquisitely sensitive to environmental perturbations and that destructive experimental manipulations rapidly and profoundly affect plant function. Since destructive measurements have been the norm in plant physiology, much of our “textbook knowledge” concerning plant physiology is unrelated to normal plant function. As such, scientists in the triad disciplines favor a more natural and holistic approach toward understanding plant function. By examining the history, philosophy, sociology and psychology of the triad disciplines, this paper refutes in eight ways the criticism that plant neurobiology presents nothing new, and that the topics of plant neurobiology fall squarely under the purview of mainstream plant physiology. It is argued that although the triad disciplines and mainstream plant physiology share the common goal of understanding plant function, they are distinct in having their own intellectual histories and epistemologies.
Plant vision is an interesting interdisciplinary branch of botany and vision science, and its emerging studies have composed an epic journey of discovery. However, there are few endeavors on modeling how a plant as an integrity sees. Inspired by the similarity between those discovered laws of plant vision and the visual performance of some insect species with compound eyes, the visual functional–structural plant modeling as a compound eye is innovatively proposed. Using this adapted basic‐pattern‐oriented modeling, we tried to validate its feasibility in terms of the structural support, visual pathway, and functional performance. First, for a diversity of woody plants, their crowns proved to show self‐similar profiles, which render the omnidirectional surfaces for structurally supporting the proposed model. Second, for many plant species, their branching proved to abide by the Pareto front, which ensures the optimality of assuming the visual pathway along the branching network. Third, in canopies the varying, but existing horizontal and vertical modes of crown shyness are detected, which in functional performance accords with the panoramic visibility of the proposed model. Overall, the feasibility of compound eye modeling is validated preliminarily, with the implication of opening a way for advancing the scientific cognition of plant vision.
Plants are not only sensitive to exogenous anaesthetics, but they also produce multitudes of endogenous substances, especially when stressed, that often have anaesthetic and anelgesic properties when applied to both humans and animals. Moreover, plants rely on neurotransmitters and their receptors for cell-cell communication and integration in a similar fashion to the use of neural systems in animals and humans. Plants also use their plant-specific sensory systems and neurotransmitter-based communication, including long-distance action potentials, to manage stress via cognition-like plant-specific behaviour and adaptation.
Viele Wege führen zum Leben – Reaktion für Reaktion werden die abiotischen Grundlagen der allerersten ökologischen Interaktion und ihrer evolutionären Entfaltung entschlüsselt. Doch wie sieht dieses Leben aus und ist es überhaupt möglich, Leben widerspruchsfrei zu definieren? Das kleinstmögliche Leben birgt das Potenzial, alles, was wir über unsere Erde und ferne Welten zu wissen glauben, größtmöglich zu verändern.
Obvious movements of plant organs have fascinated scientists for a long time. They have been studied extensively, but few behavioural studies to date have dealt with them, and hardly anything is known about their evolution. Here, we present a large experimental dataset on the stamen movement patterns found in the Loasaceae subfam. Loasoideae (Cornales). An evolutionary transition from autonomous-only to a combination of autonomous and thigmonastic stamen movement with increased complexity was experimentally demonstrated. We compare the stamen movement patterns with extensive pollinator observations and discuss it in the context of male mating behavior. Thigmonastic pollen presentation via stamen movements appears to be a crucial component of floral adaptation to pollinator behaviour, evolving in concert with complex adjustments of flower signal, reward and morphology. We hypothesize that rapid adjustments of pollen presentation timing may play a significant role in the diversificationof this plant group, representing a striking example for the evolutionary significance of plant behaviour.
Plants emerge as cognitive and intelligent organisms which coevolve with humans since the first flowering plants recognized primates as potential frugivores. Later, when humans started to settle down and initiated the agriculture, our coevolution with crop plants entered a new phase which allowed evolution of our civilization. Here we summarize recent advances in our understanding of plants relying, similarly as animals and humans, on learning and cognition to use their plant-specific behavior for survival. Although plants as such are sessile, their organs move actively and use these movements for active manipulation of their environment, both abiotic and biotic. Moreover, the major strategy of flowering plants is to control their animal pollinators and seed dispersers by providing them with food enriched not only with nutritive but also with manipulative and addictive compounds. There are several examples of cognitive supremacy of plants over animals.
Plants are highly intelligent organisms. They continuously make distributed processing of sensory information, concurrent decision making and parallel actuation. The plants are efficient green computers per se. Outside in nature, the plants are programmed and hardwired to perform a narrow range of tasks aimed to maximize the plants’ ecological distribution, survival and reproduction. To ‘persuade’ plants to solve tasks outside their usual range of activities, we must either choose problem domains which homomorphic to the plants natural domains or modify biophysical properties of plants to make them organic electronic devices. We discuss possible designs and prototypes of computing systems that could be based on morphological development of roots, interaction of roots, and analog electrical computation with plants, and plant-derived electronic components. In morphological plant processors data are represented by initial configuration of roots and configurations of sources of attractants and repellents; results of computation are represented by topology of the roots’ network. Computation is implemented by the roots following gradients of attractants and repellents, as well as interacting with each other. Problems solvable by plant roots, in principle, include shortest-path, minimum spanning tree, Voronoi diagram, -shapes, convex subdivision of concave polygons. Electrical properties of plants can be modified by loading the plants with functional nanoparticles or coating parts of plants of conductive polymers. Thus, we are in position to make living variable resistors, capacitors, operational amplifiers, multipliers, potentiometers and fixed-function generators. The electrically modified plants can implement summation, integration with respect to time, inversion, multiplication, exponentiation, logarithm, division. Mathematical and engineering problems to be solved can be represented in plant root networks of resistive or reaction elements. Developments in plant-based computing architectures will trigger emergence of a unique community of biologists, electronic engineering and computer scientists working together to produce living electronic devices which future green computers will be made of.
In a thought-provoking contribution, Baluska and Mancuso [1] resurrect the concept of plant ocelli, originally formulated over a century ago, and discuss examples of eye-like structures in cyanobacteria [2] and dinoflagellates [3] that allow these organisms to sense light direction and subsequently alter their movement. Furthermore, they put forward that two cases in higher plants suggest the occurrence of vision-like phenomena. First, the photoreceptor-mediated kin recognition in Arabidopsis thaliana, whereby plants growing with kin neighbors reorient their leaves in such a way that it decreases mutual shading (a response not observed with nonkin neighbors) [4].
Bacterial phototaxis was first recognized over a century ago, but the method by which such small cells can sense the direction of illumination has remained puzzling. The unicellular cyanobacterium Synechocystis sp. PCC 6803 moves with Type IV pili and measures light intensity and color with a range of photoreceptors. Here, we show that individual Synechocystis cells do not respond to a spatiotemporal gradient in light intensity, but rather they directly and accurately sense the position of a light source. We show that directional light sensing is possible because Synechocystis cells act as spherical microlenses, allowing the cell to see a light source and move towards it. A high-resolution image of the light source is focused on the edge of the cell opposite to the source, triggering movement away from the focused spot. Spherical cyanobacteria are probably the world's smallest and oldest example of a camera eye.
It has been known for some time that not only animals, but also some advanced unicellular algae possess imaging eyes. Now it seems that even tiny cyanobacteria have what it takes to qualify for the most basic definition of vision.
Light can penetrate several centimeters below the soil surface. Growth, development and behavior of plant roots are markedly affected by light despite their underground lifestyle. Early studies provided contrasting information on the spatial and temporal distribution of light-sensing cells in the apical region of root apex and discussed the physiological roles of plant hormones in root responses to light. Recent biological and microscopic advances have improved our understanding of the processes involved in the sensing and transduction of light signals, resulting in subsequent physiological and behavioral responses in growing root apices. Here, we review current knowledge of cellular distributions of photoreceptors and their signal transduction pathways in diverse root tissues and root apex zones. We are discussing also the roles of auxin transporters in roots exposed to light, as well as interactions of light signal perceptions with sensing of other environmental factors relevant to plant roots.
Multicellularity is often considered a prerequisite for morphological complexity, as seen in the camera-type eyes found in several groups of animals. A notable exception exists in single-celled eukaryotes called dinoflagellates, some of which have an eye-like 'ocelloid' consisting of subcellular analogues to a cornea, lens, iris, and retina. These planktonic cells are uncultivated and rarely encountered in environmental samples, obscuring the function and evolutionary origin of the ocelloid. Here we show, using a combination of electron microscopy, tomography, isolated-organelle genomics, and single-cell genomics, that ocelloids are built from pre-existing organelles, including a cornea-like layer made of mitochondria and a retinal body made of anastomosing plastids. We find that the retinal body forms the central core of a network of peridinin-type plastids, which in dinoflagellates and their relatives originated through an ancient endosymbiosis with a red alga. As such, the ocelloid is a chimaeric structure, incorporating organelles with different endosymbiotic histories. The anatomical complexity of single-celled organisms may be limited by the components available for differentiation, but the ocelloid shows that pre-existing organelles can be assembled into a structure so complex that it was initially mistaken for a multicellular eye. Although mitochondria and plastids are acknowledged chiefly for their metabolic roles, they can also be building blocks for greater structural complexity.
The ocelloid is an extraordinary eyespot organelle found only in the dinoflagellate family Warnowiaceae. It contains retina- and lens-like structures called the retinal body and the hyalosome. The ocelloid has been an evolutionary enigma because of its remarkable resemblance to the multicellular camera-type eye. To determine if the ocelloid is functionally photoreceptive, we investigated the warnowiid dinoflagellate Erythropsidinium. Here, we show that the morphology of the retinal body changed depending on different illumination conditions and the hyalosome manifests the refractile nature. Identifying a rhodopsin gene fragment in Erythropsidinium ESTs that is expressed in the retinal body by in situ hybridization, we also show that ocelloids are actually light sensitive photoreceptors. The rhodopsin gene identified is most closely related to bacterial rhodopsins. Taken together, we suggest that the ocelloid is an intracellular camera-type eye, which might be originated from endosymbiotic origin.
The halotolerant green algae Dunaliella bardawil is unique in that it accumulates under stress two types of lipid droplets: cytoplasmatic lipid droplets (CLD) and β-carotene-rich plastoglobuli (βC-plastoglobuli). Recently we isolated and analyzed the lipid and pigment compositions of these lipid droplets. Here we describe their proteome analysis. A contamination filter and an enrichment filter were utilized to define core proteins. A proteome database of D. salina/D. bardawil was constructed to aid identification of lipid droplets proteins. A total of 124 and 42 core proteins were identified in βC-plastoglobuli and in CLD, respectively, with only 8 common proteins. Dunaliella CLD resemble cytoplasmic droplets from C. reinhardtii and contain major lipid droplet associated protein (MLDP) and enzymes involved in lipid and sterol metabolism. βC-plastoglobuli proteome resembles C. reinhardtii eyespot and A. thaliana plastoglobules proteomes and contain carotene-globule-associated protein (CGP), PAP-fibrillins, SOUL heme-binding proteins, phytyl-ester synthases (PES), β-carotene biosynthesis enzymes and proteins involved in membrane remodeling/lipid droplets biogenesis: vesicle-inducing plastid protein 1 (VIPP1), synaptotagmin and the eyespot assembly proteins EYE3 and SOUL3. Based on these and previous results we propose models for biogenesis of βC-plastoglobuli, for biosynthesis of β-carotene within βC-plastoglobuli and hypothesize that βC-plastoglobuli evolved from eyespot lipid droplets.
Copyright © 2014, American Society of Plant Biologists.
Mimicry refers to adaptive similarity between a mimic organism and a model. Mimicry in animals is rather common, whereas documented cases in plants are rare, and the associated benefits are seldom elucidated [1, 2]. We show the occurrence of leaf mimicry in a climbing plant endemic to a temperate rainforest. The woody vine Boquila trifoliolata mimics the leaves of its supporting trees in terms of size, shape, color, orientation, petiole length, and/or tip spininess. Moreover, sequential leaf mimicry occurs when a single individual vine is associated with different tree species. Leaves of unsupported vines differed from leaves of climbing plants closely associated with tree foliage but did not differ from those of vines climbing onto leafless trunks. Consistent with an herbivory-avoidance hypothesis, leaf herbivory on unsupported vines was greater than that on vines climbing on trees but was greatest on vines climbing onto leafless trunks. Thus, B. trifoliolata gains protection against herbivory not merely by climbing and thus avoiding ground herbivores [3] but also by climbing onto trees whose leaves are mimicked. Unlike earlier cases of plant mimicry or crypsis, in which the plant roughly resembles a background or color pattern [4-7] or mimics a single host [8, 9], B. trifoliolata is able to mimic several hosts.
Under blue light (BL) illumination, Arabidopsis thaliana roots grow away from the light source, showing a negative phototropic response. However, the mechanism of root phototropism is still unclear. Using a noninvasive microelectrode system, we showed that the BL sensor phototropin1 (phot1), the signal transducer NONPHOTOTROPIC HYPOCOTYL3 (NPH3), and the auxin efflux transporter PIN2 were essential for BL-induced auxin flux in the root apex transition zone. We also found that PIN2-green fluorescent protein (GFP) localized to vacuole-like compartments (VLCs) in dark-grown root epidermal and cortical cells, and phot1/NPH3 mediated a BL-initiated pathway that caused PIN2 redistribution to the plasma membrane. When dark-grown roots were exposed to brefeldin A (BFA), PIN2-GFP remained in VLCs in darkness, and BL caused PIN2-GFP disappearance from VLCs and induced PIN2-GFP-FM4-64 colocalization within enlarged compartments. In the nph3 mutant, both dark and BL BFA treatments caused the disappearance of PIN2-GFP from VLCs. However, in the phot1 mutant, PIN2-GFP remained within VLCs under both dark and BL BFA treatments, suggesting that phot1 and NPH3 play different roles in PIN2 localization. In conclusion, BL-induced root phototropism is based on the phot1/NPH3 signaling pathway, which stimulates the shootward auxin flux by modifying the subcellular targeting of PIN2 in the root apex transition zone.
Flagellate green algae have developed a visual system, the eyespot apparatus, which allows the cell to phototax. In a recent proteomic approach, we identified 202 proteins from a fraction enriched in eyespot apparatuses of Chlamydomonas reinhardtii. Among these proteins, five protein kinases and two protein phosphatases were present, indicating that reversible protein phosphorylation occurs in the eyespot. About 20 major phosphoprotein bands were detected in immunoblots of eyespot proteins with an anti-phosphothreonine antibody. Toward the profiling of the targets of protein kinases in the eyespot fraction, we analyzed its phosphoproteome. The solubilized proteins of the eyespot fraction were treated with the endopeptidases LysC and trypsin prior to enrichment of phosphopeptides with immobilized metal-ion affinity chromatography. Phosphopeptides were analyzed by nano-liquid chromatography-electrospray ionization-mass spectrometry (MS) with MS/MS as well as neutral-loss-triggered MS/MS/MS spectra. We were able to identify 68 different phosphopeptides along with 52 precise in vivo phosphorylation sites corresponding to 32 known proteins of the eyespot fraction. Among the identified phosphoproteins are enzymes of carotenoid and fatty acid metabolism, putative signaling components, such as a SOUL heme-binding protein, a Ca(2+)-binding protein, and an unusual protein kinase, but also several proteins with unknown function. Notably, two unique photoreceptors, channelrhodopsin-1 and channelrhodopsin-2, contain three and one phosphorylation sites, respectively. Phosphorylation of both photoreceptors occurs in the cytoplasmatic loop next to their seven transmembrane regions in a similar distance to that observed in vertebrate rhodopsins, implying functional importance for regulation of these directly light-gated ion channels relevant for the photoresponses of C. reinhardtii.
Although cooperative interactions among kin have been established in a variety of biological systems, their occurrence in plants remains controversial.
Plants of A rabidopsis thaliana were grown in rows of either a single or multiple accessions.
Plants recognized kin neighbours and horizontally reoriented leaf growth, a response not observed when plants were grown with nonkin. Plant kin recognition involved the perception of the vertical red/far‐red light and blue light profiles. Disruption of the light profiles, mutations at the PHYTOCHROME B , CRYPTOCHROME 1 or 2, or PHOTOTROPIN 1 or 2 photoreceptor genes or mutations at the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1 gene required for auxin (growth hormone) synthesis impaired the response. The leaf‐position response increases plant self‐shading, decreases mutual shading between neighbours and increases fitness.
Light signals from neighbours are known to shape a more competitive plant body. Here we show that photosensory receptors mediate cooperative rather than competitive interactions among kin neighbours by reducing the competition for local pools of resources.
The eyespot of Chlamydomonas reinhardtii is a light-sensitive organelle important for phototactic orientation of the alga. Here, we found that eyespot size is strain specific and downregulated in light. In a strain in which the blue light photoreceptor phototropin was deleted by homologous recombination, the light regulation of the eyespot size was affected. We restored this dysfunction in different phototropin complementation experiments. Complementation with the phototropin kinase fragment reduced the eyespot size, independent of light. Interestingly, overexpression of the N-terminal light, oxygen or voltage sensing domains (LOV1+LOV2) alone also affected eyespot size and phototaxis, suggesting that aside from activation of the kinase domain, they fulfill an independent signaling function in the cell. Moreover, phototropin is involved in adjusting the level of channelrhodopsin-1, the dominant primary receptor for phototaxis within the eyespot. Both the level of channelrhodopsin-1 at the onset of illumination and its steady state level during the light period are downregulated by phototropin, whereas the level of channelrhodopsin-2 is not significantly altered. Furthermore, a light intensity-dependent formation of a C-terminal truncated phototropin form was observed. We propose that phototropin is a light regulator of phototaxis that desensitizes the eyespot when blue light intensities increase.
Die Lichtsinnesorgane der Laubblätter
- G Haberlandt
Haberlandt, G. (1905) Die Lichtsinnesorgane der Laubblätter, W. Engelmann (in German)
The perception of light in plants
- H Wagner
Wagner, H. (1909) The perception of light in plants. Ann.
Bot. 23, 459-490
Lectures on the physiology of movement in plants. V. The sense organs for gravity and light
- F Darwin
Darwin, F. (1907) Lectures on the physiology of movement
in plants. V. The sense organs for gravity and light. New
Phytol. 6, 69-76