Plant perception (physiology)

The leaf closing after touch in Mimosa pudica depends on electrical signals.
Vine tendril. Note how the plant reaches for and wraps around the galvanised wire provided for the purpose. This is a very tough twig and appears to have no other purpose than support for the plant. Nothing else grows from it. It must reach out softly, then wrap around and then dry and toughen. See more at thigmotropism.

Plant perception is the ability of plants to sense and respond to the environment to adjust their morphology, physiology, and phenotype accordingly.[1] Other disciplines such as plant physiology, ecology and molecular biology are used to assess this ability. Plants react to chemicals, gravity, light, moisture, infections, temperature, oxygen and carbon dioxide concentrations, parasite infestation, disease, physical disruption, sound,[2][3][4][5] and touch.

Processes

Detection

Displacement can be detected by plants.[6] Poplar stems can detect reorientation and inclination (equilibrioception).[7]

Pathway signals

Wounded tomatoes are known to produce the volatile odour methyl jasmonate as an alarm signal.[8] Neighbouring plants can then detect the chemical and prepare for the attack by producing chemicals that defend against insects or attract predators.[8]

Plants systematically use hormonal signalling pathways to coordinate their own development and morphology.

Neurochemicals

Plants produce several proteins found in the animal neuron systems such as acetylcholine esterase, glutamate receptors, GABA receptors, and endocannabinoid signaling components. They also use ATP, NO, and ROS like animals for signaling.[9]

Electrophysiology

Although plant cells are not neurons, they can be electrically excitable and can display rapid electrical responses (action potentials) to environmental stimuli. These action potentials can influence processes such as actin-based cytoplasmic streaming, plant organ movements, wound responses, respiration, photosynthesis, and flowering.[10][11][12][13] These electrical responses can cause the synthesis of numerous organic molecules, including ones that act as neuroactive substances in other organisms. Thus, plants accomplish behavioural responses in environmental, communicative, and ecological contexts.

Signal response

A plant's concomitant reactive behavior is mediated by phytochromes, kinins, hormones, antibiotic or other chemical release, changes of water and chemical transport, and other means. These responses are generally slow, taking at minimum a number of hours to accomplish, and can best be observed with time-lapse cinematography, but rapid movements can occur as well. Plants respond to volatile signals produced by other plants.[14][15] Jasmonate levels also increase rapidly in response to mechanical perturbations such as tendril coiling.[16]

Plants have many strategies to fight off pests. For example, they can produce different toxins (phytoalexins) against invaders or they can induce rapid cell death in invading cells to hinder the pests from spreading out.

Some plants are capable of rapid movement: the mimosa plant (Mimosa pudica) makes its thin leaves point down at the slightest touch and carnivorous plants such as the Venus flytrap snap shut by the touch of insects. In the Venus flytrap, touch is detected by cilia that generate an action potential that stimulates motor cells, by which movement occurs.[17]

In plants, the mechanism responsible for adaptation is signal transduction.[18][19][20][21]

Adaptive responses include:

Aspects of perception

Light

The sunflower, a common heliotropic plant which perceives and reacts to sunlight by slow turning movement

Many plant organs contain photo-sensitive compounds (phototropins, cryptochromes and phytochromes), each reacting very specifically to certain wavelengths of light. These light sensors tell the plant if it is day or night, how long the day is, how much light is available and from where the light comes. Shoots grow towards light and roots usually grow away from light. These responses are called phototropism and skototropism respectively. They are brought about by light sensitive pigments like phototropins and phytochromes and the plant hormone auxin. Many plants exhibit certain phenomena at specific times of the day; for example, certain flowers open only in the mornings. Plants keep track of the time of day with a circadian clock. This internal clock is set to solar time every day using sunlight, temperature and other cues, similar to the biological clocks of other organisms. The internal clock coupled with the ability to perceive light also allows plants to measure the time of the day and so find the season of the year. This is how many plants know when to flower. (see photoperiodism) The seeds of many plants sprout only after they are exposed to light. This response is carried out by phytochrome signalling. Plants are also able to sense the quality of light and respond appropriately. For example, in low light conditions, plants produce more photosynthetic pigments. If the light is very bright or if the levels of harmful UV increase, plants produce more of their protective pigments that act as sunscreens.[29]

Gravity

To orient themselves correctly, plants must have an adequate sense of the direction of gravity’s unidirectional pull. The subsequent response plant movement is known as gravitropism. Typically, in the root this works as gravity is sensed and translated in the root tip, and subsequently roots grow towards gravity via elongation of the cells. In the shoot, similar effects are happening, but gravity is perceived and then growth occurs in the opposite direction, as the above ground part of the plant experiences negative gravitropism.[30]

At the root tip, there are amyloplasts containing starch granules that fall in the direction of gravity. This weight activates secondary receptors, which signal to the plant the direction of gravitational pull. After this occurs, auxin is redistributed through polar auxin transport and differential growth towards gravity begins. In the shoots, auxin redistribution occurs in a way to produce differential growth away from gravity.

For perception to happen, the plant must sense, perceive and translate the direction of gravity. Without gravity, proper orientation will not occur and the plant will not effectively grow. The root will not be able to uptake nutrients or water, and the shoot will not grow towards the sky to maximize photosynthesis.[31]

Plant intelligence

Plants do not have a brain or neuronal network, but reactions within signalling pathways may provide a biochemical basis for learning and memory in addition to computation and problem solving.[32] Controversially, the brain is used as a metaphor in plant intelligence to provide an integrated view of signalling.[33]

Plants respond to environmental stimuli by movement and changes in morphology. They communicate while actively competing for resources. In addition, plants accurately compute their circumstances, use sophisticated cost–benefit analysis and take tightly controlled actions to mitigate and control diverse environmental stressors. Plants are also capable of discriminating positive and negative experiences and of learning by registering memories from their past experiences.[34][35][36][37][38] Plants use this information to update their behaviour in order to survive present and future challenges of their environment.

Plant physiology studies the role of signalling to integrate data obtained at the genetic, biochemical, cellular and physiological levels to understand plant development and behaviour. The neurobiological view sees plants as information-processing organisms with rather complex processes of communication occurring throughout the individual plant organism. It studies how environmental information is gathered, processed, integrated and shared (sensory plant biology) to enable these adaptive and coordinated responses (plant behaviour); and how sensory perceptions and behavioural events are 'remembered' in order to allow predictions of future activities upon the basis of past experiences. Plants, it is claimed by some plant physiologists, are as sophisticated in behaviour as animals but this sophistication has been masked by the time scales of plants' response to stimuli, many orders of magnitude slower than animals'.

It has been argued that although plants are capable of adaptation, it should not be called intelligence, as plant neurobiologists are relying primarily on metaphors and analogies to argue that complex responses in plants can only be produced by intelligence.[39] "A bacterium can monitor its environment and instigate developmental processes appropriate to the prevailing circumstances, but is that intelligence? Such simple adaptation behaviour might be bacterial intelligence but is clearly not animal intelligence."[40] However, plant intelligence fits a definition of intelligence proposed by David Stenhouse in a book about evolution and animal intelligence where he described it as "adaptively variable behaviour during the lifetime of the individual".[41] Critics of the concept have also argued that a plant cannot have goals once it is past the development stage of seedling because, as a modular organism, each module seeks its own survival goals and the resulting organism level behavior is not centrally controlled.[40] This view, however, necessarily accommodates the possibility that a tree is a collection of individually intelligent modules cooperating, competing and influencing each other to determine behavior in a bottom-up fashion. The development into a larger organism whose modules must deal with different environmental conditions and challenges is not universal across plant species however, as smaller organisms might be subject to the same conditions across their bodies, at least, when the below and above ground parts are considered separately. Moreover, the claim that central control of development is completely absent from plants is readily falsified by apical dominance.

The Italian botanist Federico Delpino wrote on the idea of plant intelligence in 1867.[42] Charles Darwin studied the movement of plants and in 1880 published a book The Power of Movement in Plants. In the book he concludes:

It is hardly an exaggeration to say that the tip of the radicle thus endowed [..] acts like the brain of one of the lower animals; the brain being situated within the anterior end of the body, receiving impressions from the sense-organs, and directing the several movements.

In philosophy, there are few studies of the implications of plant perception. Michael Marder put forth a phenomenology of plant life based on the physiology of plant perception.[43] Paco Calvo Garzon offers a philosophical take on plant perception based on the cognitive sciences and the computational modeling of consciousness.[44]

Comparison to neurobiology

A plant's sensory and response system has been compared to the neurobiological processes of animals. Plant neurobiology, an unfamiliar misnomer, concerns mostly the sensory adaptive behaviour of plants and plant electrophysiology. Indian scientist J. C. Bose is credited as the first person to research and talk about neurobiology of plants. Many plant scientists and neuroscientists, however, view this as inaccurate, because plants do not have neurons.[39]

The ideas behind plant neurobiology were criticised in a 2007 article[39] published in Trends in Plant Science by Amedeo Alpi and 35 other scientists, including such eminent plant biologists as Gerd Jürgens, Ben Scheres, and Chris Sommerville. The breadth of fields of plant science represented by these researchers reflects the fact that the vast majority of the plant science research community reject plant neurobiology. Their main arguments are that:[39]

  • "Plant neurobiology does not add to our understanding of plant physiology, plant cell biology or signaling".
  • "There is no evidence for structures such as neurons, synapses or a brain in plants".
  • The common occurrence of plasmodesmata in plants which "poses a problem for signaling from an electrophysiological point of view" since extensive electrical coupling would preclude the need for any cell-to-cell transport of a ‘neurotransmitter-like’ compounds.

The authors call for an end to "superficial analogies and questionable extrapolations" if the concept of "plant neurobiology" is to benefit the research community.[39]

There were several responses to the criticism clarifying that the term "plant neurobiology" is a metaphor and metaphors have proved useful on several previous occasions.[45][46] Plant ecophysiology describes this phenomenon.

Parallels in other taxa

As described above in the case of a plant, similar mechanisms exist in a bacterial cell, a choanoflagellate, a fungal hypha, or a sponge, among the many other examples. All of these individual organisms of the respective taxa, despite being devoid of a brain or nervous system, are capable of sensing their immediate and momentary environment and responding accordingly. In the case of single-celled life, the sensory pathways are even more primitive in the sense that they take place on the surface of a single cell, as opposed to a network of many cells.

See also

References

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Further reading

  • Baluška F (ed) (2009). Plant-Environment Interactions: From Sensory Plant Biology to Active Plant Behavior. Springer Verlag.
  • Brenner ED, Stahlberg R, Mancuso S, Vivanco J, Baluska F, Van Volkenburgh E (August 2006). "Plant neurobiology: an integrated view of plant signaling". Trends in Plant Science. 11 (8): 413–9. doi:10.1016/j.tplants.2006.06.009. PMID 16843034.
  • Cvrcková F, Lipavská H, Zárský V (May 2009). "Plant intelligence: why, why not or where?". Plant Signaling & Behavior. 4 (5): 394–9. doi:10.4161/psb.4.5.8276. PMC 2676749. PMID 19816094.
  • Garzón FC (July 2007). "The quest for cognition in plant neurobiology". Plant Signaling & Behavior. 2 (4): 208–11. doi:10.4161/psb.2.4.4470. PMC 2634130. PMID 19516990.
  • Gilroy S, Masson PH (2007). Plant Tropisms. Iowa State University Press.
  • Karban R (July 2008). "Plant behaviour and communication". Ecology Letters. 11 (7): 727–39. doi:10.1111/j.1461-0248.2008.01183.x. PMID 18400016.
  • Karban R (2015). Plant Sensing and Communication. University of Chicago Press.
  • Mancuso S, Shabala S (2006). Rhythms in Plants. Springer Verlag.
  • Manetas, Yiannis (2012). "Are Plants Intelligent Organisms After All?". Alice in the Land of Plants. Berlin, Heidelberg: Springer Berlin Heidelberg. doi:10.1007/978-3-642-28338-3_10. ISBN 978-3-642-28337-6.
  • Scott P (2008). Physiology and Behaviour of Plants. John Willey & Sons Ltd.
  • Trewavas A (July 2003). "Aspects of plant intelligence". Annals of Botany. 92 (1): 1–20. doi:10.1093/aob/mcg101. PMC 4243628. PMID 12740212.
  • Trewavas A (September 2005). "Plant intelligence". Die Naturwissenschaften. 92 (9): 401–13. Bibcode:2005NW.....92..401T. doi:10.1007/s00114-005-0014-9. PMID 16142448.
  • Trewavas A (June 2009). "What is plant behaviour?". Plant, Cell & Environment. 32 (6): 606–16. doi:10.1111/j.1365-3040.2009.01929.x. PMID 19143994.
  • Volkov AG (2006). Plant Electrophysiology. Springer Verlag.
  • Volkov AG, Carrell H, Adesina T, Markin VS, Jovanov E (July 2008). "Plant electrical memory". Plant Signaling & Behavior. 3 (7): 490–2. doi:10.4161/psb.3.7.5684. PMC 2634440. PMID 19704496.
  • Keen NT, Mayama S, Leach JE, Tsujumu S, eds. (2001). Delivery and Perception of Pathogen Signals in Plants. APS Press. p. 268. ISBN 0-89054-259-7.
  • Taiz L, Zeiger E (2006). Plant Physiology, fourth edition. Sinauer Associates. p. 700 (est). ISBN 0-87893-856-7.
  • Miller D, Hable W, Gottwald J, Ellard-Ivey M, Demura T, Lomax T, Carpita N (December 1997). "Connections: the hard wiring of the plant cell for perception, signaling, and response". The Plant Cell. 9 (12): 2105–17. PMC 157061. PMID 9437857.
  • Scheel D, Wastermack C (May 2002). Plant Signal Transduction. Oxford University Press. p. 346. ISBN 978-0-19-963879-6. Retrieved 2006-12-25.
  • Taiz L, Zeiger E (2002). Plant Physiology Online: A companion to Plant Physiology (Third ed.). Sinauer Associates. Archived from the original on 7 December 2006. Retrieved 2006-12-26.

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