Plant cognition

Plant cognition or plant gnosophysiology^[1] is the study of the learning and memory of plants, exploring the idea it is not only animals that are capable of detecting, responding to and learning from internal and external stimuli in order to choose and make decisions that are most appropriate to ensure survival. Over recent years, experimental evidence for the cognitive nature of plants has grown rapidly and has revealed the extent to which plants can use senses and cognition to respond to their environments.^[2] Some researchers claim that plants process information in similar ways as animal nervous systems.^[3]^[4] The implications are contested; whether plants have cognition or are simply animated objects.

History

The idea of cognition in plants was first explored by Charles Darwin in the late 1800s in the book The Power of Movement in Plants, co-authored with his son Francis. Using a neurological metaphor, he described the sensitivity of plant roots in proposing that the tip of roots acts like the brain of some lower animals. This involves reacting to sensation in order to determine their next movement^[5] even though plants possess neither brains nor nerves.

Irrespective of whether this neurological metaphor is correct or, more generally, the modern application of neuroscience terminology and concepts to plants is appropriate, the Darwinian idea of the root tip of plants functioning as a "brain-like" organ (together with the so-called "root-brain hypothesis") has experienced an ongoing revival in plant physiology.^[6]

While plant "neurobiology" focuses on the physiological study of plants, modern plant cognition primarily applies a behavioural/ecological approach. Today, plant cognition is emerging as a field of research directed at experimentally testing the cognitive abilities of plants, including perception, learning processes, memory and consciousness.^[7] This framework holds considerable implications for the way we perceive plants as it redefines the traditionally held boundary between animals and plants.^[8]

Types

The study of plant cognition stems from the idea that plants are able to learn and adapt to their environment with only a stimulus, integration, and response system. While proven that plants do indeed lack a brain and the function of a conscious working nervous system, plants are still somehow capable of adapting to their environment and changing the integration pathway that would ultimately lead to how a plant “decides” to take response to a presented stimulus.^[9] This raises issues of plant intelligence which is defined to be able to actively adapt to any stimulus presented to the species from the environment.^[10]^{[failed verification]} Plants are therefore clever in sensing the environmental stimulus e.g. young sunflowers that face the sun for their growth.

Plant memory

In a study done by Monica Gagliano from the University of Western Australia’s Centre for Evolutionary Biology, Mimosa pudica (sensitive plant) was tested for habituation to repeatedly being dropped. After multiple drops, it was found that the plants eventually became habituated, opening their leaves more quickly compared to the first time they were dropped.^[11] While the mechanism of this plant behavior is still not fully understood, it is strongly linked to changes in the flux within calcium channels.^[12]

Another example of short term "memory" of a plant is found in the Venus flytrap, whose rapid closure is only triggered when at least two trap hairs are contacted within twenty seconds of one another. One hypothesis that explains how this occurs is by electrical signalling in plants. When one trap hair (mechanoreceptor) is triggered, a sub-threshold potential is reached. When two trap hairs are triggered, a threshold is reached, generating an action potential that closes the trap.^{[citation needed]}

Associative learning

In 2016, a research team led by Monica Gagliano set out to test whether plants learn to respond to predicted events in their environment. The research demonstrated that plants were capable of learning the association between the occurrence of one event and the anticipation of another event (i.e. Pavlovian learning).^[13] By experimentally demonstrating associative learning in plants, this finding qualified plants as proper subjects of cognitive research.^[13] In this study, it was hypothesized that plants have the capability to associate one type of stimulus with another. To test this hypothesis, pea plants were exposed to two different stimuli. For the training phase, one group of pea plants was exposed to both wind and light, and the other group of plants was exposed to wind without light as a control. In the experimental phase, the plants were exposed only to the wind stimulus. The pea plants that were only ever exposed to wind without light grew away from the wind in both the training and experimental phases. In contrast, the pea plants exposed to both wind and light in the training phase exhibited growth toward a wind stimulus without the presence of light, demonstrating an apparent learned association between wind and light. The mechanism for this response is not entirely understood, though it is hypothesized that sensory inputs from mechanoreceptors and photoreceptors were somehow integrated within the plants. This explains why a non-light stimulus would trigger a growth response in the trained pea plant that is typically only triggered by the activation of photoreceptors.^[14]

A replication study with a larger sample size, published in 2020, found no evidence of associative learning in pea plants.^[15] However, it also failed to replicate the finding that light functioned effectively as an unconditioned stimulus. Pea plants in this study displayed only a slight trend rather than a reliable directional growth response towards previously presented light. The replicated experimental setup differed from the original in the presence of higher levels of ambient and reflected light, which may have randomised directional growth somewhat and prevented replication.^[16]

Further research

In 2003, Anthony Trewavas led a study to see how the roots interact with one another and study their signal transduction methods. He was able to draw similarities between water stress signals in plants affecting developmental changes and signal transductions in neural networks causing responses in muscle.^[17] Particularly, when plants are under water stress, there are abscisic acid dependent and independent effects on development.^[18] This brings to light further possibilities of plant decision-making based on its environmental stresses. The integration of multiple chemical interactions show evidence of the complexity in these root systems.^[19]

In 2012, Paco Calvo Garzón and Fred Keijzer speculated that plants exhibited structures equivalent to (1) action potentials (2) neurotransmitters and (3) synapses. Also, they stated that a large part of plant activity takes place underground, and that the notion of a 'root brain' was first mooted by Charles Darwin in 1880. Free movement was not necessarily a criterion of cognition, they held. The authors gave five conditions of minimal cognition in living beings, and concluded that 'plants are cognitive in a minimal, embodied sense that also applies to many animals and even bacteria.'^[3] In 2017 biologists from University of Birmingham announced that they found a "decision-making center" in the root tip of dormant Arabidopsis seeds.^[20]

In 2014, Anthony Trewavas released a book called Plant Behavior and Intelligence that highlighted a plant's cognition through its colonial-organization skills reflecting insect swarm behaviors.^[21] This organizational skill reflects the plant's ability to interact with its surroundings to improve its survivability, and a plant's ability to identify exterior factors. Evidence of the plant's minimal cognition of spatial awareness can be seen in their root allocation relative to neighboring plants.^[22] The organization of these roots have been found to originate from the root tip of plants.^[23]

On the other hand, Dr. Crisp and his colleagues proposed a different view on plant memory in their review: plant memory could be advantageous under recurring and predictable stress; however, resetting or forgetting about the brief period of stress may be more beneficial for plants to grow as soon as the desirable condition returns.^[24]

Affifi (2018) proposed an empirical approach to examining the ways plants model coordinate goal-based behaviour to environmental contingency as a way of understanding plant learning.^[25] According to this author, associative learning will only demonstrate intelligence if it is seen as part of teleologically integrated activity. Otherwise, it can be reduced to mechanistic explanation.

Raja et al (2020) found that potted French bean plants, when planted 30 centimetres from a garden cane, would adjust their growth patterns to enable themselves to use the cane as a support in the future. Raja later stated that "If the movement of plants is controlled and affected by objects in their vicinity, then we are talking about more complex behaviours (rather than simple) reactions". Raja proposed that researchers should look for corresponding cognitive signatures.^[26]^[27]

In 2017 Yokawa, K. et al. found that, when exposed to anesthetics, a number of plants lost both their autonomous and touch-induced movements. Venus flytraps no longer generate electrical signals and their traps remain open when trigger hairs were touched, and growing pea tendrils stopped their autonomous movements and were immobilized in a curled shape.^[28]

Criticism

The idea of plant cognition is a source of controversy.

Amadeo Alpi and 35 other scientists published an article in 2007 titled "Plant Neurobiology: No Brain, No Gain?" in Trends in Plant Science.^[29] In this article, they argue that since there is no evidence for the presence of neurons in plants, the idea of plant neurobiology and cognition is unfounded and needs to be redefined. In response to this article, Francisco Calvo Garzón published an article in Plant Signaling and Behavior.^[9] He states that, while plants do not have "neurons" as animals do, they do possess an information-processing system composed of cells. He argues that this system can be used as a basis for discussing the cognitive abilities of plants.

References

^ Michmizos, Dimitrios; Hilioti, Zoe (January 2019). "A roadmap towards a functional paradigm for learning & memory in plants". Journal of Plant Physiology. 232: 209–215. Bibcode:2019JPPhy.232..209M. doi:10.1016/j.jplph.2018.11.002. PMID 30537608. S2CID 56178258.
^ Gagliano M (November 2014). "In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants". AoB Plants. 7. doi:10.1093/aobpla/plu075. PMC 4287690. PMID 25416727.
^ ^a ^b Garzon P, Keijzer F (2011). "Plants: Adaptive behavior, root-brains, and minimal cognition" (PDF). Adaptive Behavior. 19 (3): 155–171. doi:10.1177/1059712311409446. S2CID 5060470.
^ Karban R (July 2008). "Plant behaviour and communication". Ecology Letters. 11 (7): 727–39. Bibcode:2008EcolL..11..727K. doi:10.1111/j.1461-0248.2008.01183.x. PMID 18400016.
^ Darwin, C. (1880). The Power of Movement in Plants. London: John Murray. Darwin Online : "The course pursued by the radicle in penetrating the ground must be determined by the tip; hence it has acquired such diverse kinds of sensitiveness. It is hardly an exaggeration to say that the tip of the radicle thus endowed, and having the power of directing the movements of the adjoining parts, acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense-organs, and directing the several movements."
^ "ABOUT US - Plant Signaling and Behavior". Plant Signaling and Behavior. Retrieved 2017-03-25.
^ Pollan M (23 December 2013). "The Intelligent Plant". michaelpollan.com. The New Yorker. Retrieved 2019-03-08.
^ "Monica Gagliano - the science of plant behaviour and consciousness". Monica Gagliano - the science of plant behaviour and consciousness. Retrieved 2017-03-25.
^ ^a ^b Garzón FC (July 2007). "The quest for cognition in plant neurobiology". Plant Signaling & Behavior. 2 (4): 208–11. Bibcode:2007PlSiB...2..208C. doi:10.4161/psb.2.4.4470. PMC 2634130. PMID 19516990.
^ Stenhouse, David (1974) [1973]. The Evolution of Intelligence: A General Theory and Some of Its Implications. New York: George Allen & Unwin (Barnes & Noble Books). pp. 364–365. ISBN 006496518X. OCLC 1057540.
^ Gagliano M, Renton M, Depczynski M, Mancuso S (May 2014). "Experience teaches plants to learn faster and forget slower in environments where it matters". Oecologia. 175 (1): 63–72. Bibcode:2014Oecol.175...63G. doi:10.1007/s00442-013-2873-7. PMID 24390479. S2CID 5038227.
^ Cahill J, Bao T, Maloney M, Kolenosky C (June 4, 2012). "Mechanical leaf damage causes localized, but not systemic, changes in leaf movement behavior of the Sensitive Plant, Mimosa pudica". Botany. doi:10.1139/cjb-2012-0131.
^ ^a ^b Gagliano M, Vyazovskiy VV, Borbély AA, Grimonprez M, Depczynski M (December 2016). "Learning by Association in Plants". Scientific Reports. 6 (1): 38427. Bibcode:2016NatSR...638427G. doi:10.1038/srep38427. PMC 5133544. PMID 27910933.
^ Mawphlang OI, Kharshiing EV (July 11, 2017). "Photoreceptor Mediated Plant Growth Responses: Implications for Photoreceptor Engineering toward Improved Performance in Crops". Frontiers in Plant Science. 8: 1181. doi:10.3389/fpls.2017.01181. PMC 5504655. PMID 28744290.
^ Markel K (June 2020). "Lack of evidence for associative learning in pea plants". eLife. 9: e57614. doi:10.7554/eLife.57614. PMC 7311169. PMID 32573434.
^ Gagliano, Monica; Vyazovskiy, Vladyslav V; Borbély, Alexander A; Depczynski, Martial; Radford, Ben (2020-09-10). Lee, Daeyeol; Hardtke, Christian S (eds.). "Comment on 'Lack of evidence for associative learning in pea plants'". eLife. 9: e61141. doi:10.7554/eLife.61141. ISSN 2050-084X. PMC 7556858. PMID 32909941.
^ Trewavas A (July 2003). "Aspects of plant intelligence". Annals of Botany. 92 (1): 1–20. doi:10.1093/aob/mcg101. PMC 4243628. PMID 12740212.
^ Shinozaki K (2000). "Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways". Current Opinion in Plant Biology. 3 (3): 217–223. doi:10.1016/s1369-5266(00)00067-4. PMID 10837265.
^ McCully ME (June 1999). "ROOTS IN SOIL: Unearthing the Complexities of Roots and Their Rhizospheres". Annual Review of Plant Physiology and Plant Molecular Biology. 50: 695–718. doi:10.1146/annurev.arplant.50.1.695. PMID 15012224.
^ Topham AT, Taylor RE, Yan D, Nambara E, Johnston IG, Bassel GW (June 2017). "Temperature variability is integrated by a spatially embedded decision-making center to break dormancy in Arabidopsis seeds". Proceedings of the National Academy of Sciences of the United States of America. 114 (25): 6629–6634. Bibcode:2017PNAS..114.6629T. doi:10.1073/pnas.1704745114. PMC 5488954. PMID 28584126.
^ Trewavas 2014, p. 95-96.
^ Calvo Garzón P, Keijzer F (June 2011). "Plants: Adaptive behavior, root-brains, and minimal cognition" (PDF). Adaptive Behavior. 19 (3): 155–71. doi:10.1177/1059712311409446. S2CID 5060470.
^ Trewavas 2014, p. 140.
^ Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ (February 2016). "Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics". Science Advances. 2 (2): e1501340. Bibcode:2016SciA....2E1340C. doi:10.1126/sciadv.1501340. PMC 4788475. PMID 26989783.
^ Affifi R (2018). "Deweyan Psychology in Plant Intelligence Research: Transforming Stimulus and Response". In Baluska F, Gagliano M, Witzany G (eds.). Memory and Learning in Plants. Signaling and Communication in Plants. Cham.: Springer. pp. 17–33. doi:10.1007/978-3-319-75596-0_2. ISBN 978-3-319-75595-3.
^ "Plants: Are they conscious?". BBC Science Focus Magazine. 5 February 2021. Retrieved 6 February 2021.
^ Raja, Vicente; Silva, Paula L.; Holghoomi, Roghaieh; Calvo, Paco (December 2020). "The dynamics of plant nutation". Scientific Reports. 10 (1): 19465. Bibcode:2020NatSR..1019465R. doi:10.1038/s41598-020-76588-z. PMC 7655864. PMID 33173160.
^ Yokawa, K; Kagenishi, T; Pavlovič, A; Gall, S; Weiland, M; Mancuso, S; Baluška, F (11 December 2017). "Anaesthetics stop diverse plant organ movements, affect endocytic vesicle recycling and ROS homeostasis, and block action potentials in Venus flytraps". Annals of Botany. 122 (5): 747–756. doi:10.1093/aob/mcx155. PMC 6215046. PMID 29236942.
^ Alpi A, Amrhein N, Bertl A, Blatt MR, Blumwald E, Cervone F, et al. (April 2007). "Plant Neurobiology: No Brain, No Gain?". Trends in Plant Science. 12 (4): 135–6. Bibcode:2007TPS....12..135A. doi:10.1016/j.tplants.2007.03.002. PMID 17368081.