Abstract
The nervous system of animals serves the acquisition, memorization and recollection of information. Like animals, plants also acquire a huge amount of information from their environment, yet their capacity to memorize and organize learned behavioral responses has not been demonstrated. In Mimosa pudica—the sensitive plant—the defensive leaf-folding behaviour in response to repeated physical disturbance exhibits clear habituation, suggesting some elementary form of learning. Applying the theory and the analytical methods usually employed in animal learning research, we show that leaf-folding habituation is more pronounced and persistent for plants growing in energetically costly environments. Astonishingly, Mimosa can display the learned response even when left undisturbed in a more favourable environment for a month. This relatively long-lasting learned behavioural change as a result of previous experience matches the persistence of habituation effects observed in many animals.
Similar content being viewed by others
References
Allis CD, Jenuwein T, Reinberg D, Caparros ML (2007) Epigenetics. Cold Spring Harbor Laboratory Press, New York
Alvarez ME, Nota F, Cambiagno DA (2010) Epigenetic control of plant immunity. Mol Plant Pathol 11:563–576
Applewhite PB (1972) Behavioral plasticity in the sensitive plant, Mimosa. Behav Biol 7:47–53
Baldwin IT, Schmelz EA (1996) Immunological “memory” in the induced accumulation of nicotine in wild tobacco. Ecology 77:236–246
Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4
Bauer EP, Schafe GE, LeDoux JE (2002) NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 22:5239–5249
Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Bio 1:11–21
Bose I, Karmakar R (2008) Simple models of plant learning and memory. Phys Script T106:9–12
Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72
Braam J (2005) In touch: plant responses to mechanical stimuli. New Phytol 165:373–389
Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information-theoretic approach. Springer, New York
Cahill JF Jr, Bao T, Maloney M, Kolenosky C (2013) Mechanical leaf damage causes localized, but not systematic, changes in leaf movement behaviour of the sensitive plant, Mimosa pudica. Botany 91:43–47
Chakravarthy SV, Ghosh J (1997) On Hebbian-like adaptation in heart muscle: a proposal for ‘cardiac memory’. Biol Cybern 76:207–215
Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139
Conrath U (2009) Priming of induced plant defense responses. Adv Bot Res 51:361–395
Conrath U, Thulke O, Katz V, Schwindling S, Kohler A (2001) Priming as a mechanism in induced systemic resistance of plants. Eur J Plant Pathol 107:113–119
Crawley MJ (2007) The R book. Wiley, Chichester
Cvrčková F, Lipavská H, Žárský V (2009) Plant intelligence: why, why not or where? Plant Signal Behav 4:394–399
Demongeot J, Thomas R, Thellier M (2000) A mathematical model for storage and recall functions in plants. C R Acad Sci III 323:93–97
Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun 3:740
Dostál R (1967) On integration in plants. Harvard University Press, Cambridge
Dukas R (2004) Evolutionary biology of animal cognition. Annu Rev Ecol Evol Syst 35:347–374
Eisenstein EM, Eisenstein D, Smith JC (2001) The evolutionary significance of habituation and sensitization across phylogeny: a behavioural homeostasis model. Integr Phys Behav Sci 36:251–265
Eisner T (1981) Leaf folding in a sensitive plant: a defensive thorn-exposure mechanism. Proc Natl Acad Sci USA 78:402–404
Esdin J, Pearce K, Glanzman DL (2010) Long-term habituation of the gill-withdrawal reflex in Aplysia requires gene transcription, calcineurin and L-type voltage-gated calcium channels. Front Behav Neurosci 4:181
Fleurat-Lessard P, Bouche-Pillion S, Leloup C, Bonnemain J (1997) Distribution and activity of the plasma membrane H+-ATPase related to motor cell function in Mimosa pudica L. Plant Physiol 114:827–834
Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257
Gális I, Gaquerel E, Pandey SP, Baldwin IT (2009) Molecular mechanisms underlying plant memory in JA-mediated defence responses. Plant Cell Environ 32:617–627
Giles AC, Rankin CH (2009) Behavioral and genetic characterization of habituation using Caenorhabditis elegans. Neurobiol Learn Mem 92:139–146
Ginsburg S, Jablonka E (2009) Epigenetic learning in non-neural organisms. J Biosci 33:633–646
Glanzman DL (2009) Habituation in Aplysia: the Cheshire cat of neuro-biology. Neurobiol Learn Mem 92:147–154
Goodrich J, Tweedie S (2002) Remembrance of things past: chromatin remodeling in plant development. Annu Rev Cell Dev Biol 18:707–746
Grissom N, Bhatnagar S (2009) Habituation to repeated stress: get used to it. Neurobiol Learn Mem 92:215–224
Halling BD, Aracena-Parks P, Hamilton SL (2005) Regulation of voltage-gated Ca2+ channels by calmodulin. Sci STKE 315:15. doi:10.1126/stke.3152005re15
Han S-K, Wagner D (2013) Role of chromatin in water stress responses in plants. J Exp Bot. doi:10.1093/jxb/ert403
Hemmi JM, Merkle T (2009) High stimulus specificity characterizes anti-predator habituation under natural conditions. Proc R Soc B 276:4381–4388
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stat Circ 347:1–32
Hoddinott J (1997) Rates of translocation and photosynthesis in Mimosa pudica L. New Phytol 79:269–272
Inoue J (2008) A simple Hopfield-like cellular network model of plant intelligence. Prog Brain Res 168:169–174
Jensen EL, Dill LM, Cahill JF Jr (2011) Applying behavioral-ecological theory to plant defense: light-dependent movement in Mimosa pudica suggests a trade-off between predation risk and energetic reward. Am Nat 177:377–381
Karban R (2008) Plant behaviour and communication. Ecol Lett 11:727–739
Karban R, Niiho C (1995) Induced resistance and susceptibility to herbivory: plant memory and altered plant development. Ecology 76:1220–1225
Kawecki TJ (2010) Evolutionary ecology of learning: insights from fruit flies. Popul Ecol 52:15–25
Kenzer AL, Ghezzi PM, Fuller T (2013) Stimulus specificity and dishabituation of operant responding in humans. J Exp Anal Behav 100:61–78
Kim MC, Chung WS, Yun D-J, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21
Kinoshita T, Jacobsen SE (2012) Opening the door to epigenetics in PCP. Plant Cell Physiol 53:763–765
Krasne FB, Teshiba TM (1995) Habituation of an invertebrate escape reflex due to modulation by higher centers rather than local events. Proc Natl Acad Sci USA 92:3362–3366
Ledón-Rettig CC, Richards CL, Martin LB (2013) Epigenetics for behavioral ecologists. Behav Ecol 24:311–324
Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Study Behav 227:215–290
Limback-Stokin K, Korzus E, Nagaoka-Yasuda R, Mayford M (2004) Nuclear calcium/calmodulin regulates memory consolidation. J Neurosci 24:10858–10867
Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 422:1046–1049
Moran N (2007) Osmoregulation of leaf motor cells. FEBS Lett 581:2337–2347
Okano H, Hirano T, Balaban E (2000) Learning and memory. Proc Natl Acad Sci USA 97:12403–12404
Pecinka A, Mittelsten Scheid O (2012) Stress-induced chromatin changes: a critical view on their heritability. Plant Cell Physiol 53:801–808
Perisse E, Raymond-Delpech V, Neant I, Matsumoto Y, Leclerc C, Moreau M, Sandoz JC (2009) Early calcium increase triggers the formation of olfactory long-term memory in honeybees. BMC Biol 7:30. doi:10.1186/1741-7007-7-30
Petrinovich L, Widaman KF (1984) An evaluation of statistical strategies to analyse repeated-measures data. In: Peeke HVS, Petrinovich L (eds) Habituation, sensitization, and behaviour. Academic Press, New York, pp 155–201
Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, et al. (2009) Habituation revisited: an updated and revised description of the behavioural characteristics of habituation. Neurobiol Learn Mem 92:135–138
Reyes JC, Hennig L, Gruissem W (2002) Chromatin-remodeling and memory factors. New regulators of plant development. Plant Physiol 130:1090–1101
Roshchina VV (2001) Neurotransmitters in plant life. Science Publishers, Enfield
Ruuhola T, Salminen JP, Haviola S, Yang S, Rantala MJ (2007) Immunological memory of mountain birches: effects of phenolics on performance of the autumnal moth depend on herbivory history of trees. J Chem Ecol 33:1160–1176
Shepherd VA (2012) At the root of plant neurobiology. In: Volkov AG (ed) Plant electrophysiology. Springer, Berlin, pp 3–43
Sung S, Amasino MR (2004) Vernalisation and epigenetics: how plants remember winter. Curr Opin Plant Biol 7:4–10
Sztarker J, Tomsic D (2011) Brain modularity in arthropods: individual neurons that support “what” but not “where” memories. J Neurosci 31:8175–8180
Thellier M, Lüttge U (2013) Plant memory: a tentative model. Plant Biol 15:1–12
Thellier M, Desbiez MO, Champagnat P, Kergosien Y (1982) Do memory processes occur also in plants? Physiol Plant 56:281–284
Thellier M, Le Sceller L, Norris V, Verdus MC, Ripoll C (2000) Long-distance transport, storage and recall of morphogenetic information in plants: the existence of a primitive plant “memory”. C R Acad Sci III 323:81–91
Thompson RF (2009) Habituation: a history. Neurobiol Learn Mem 92:127–134
Thorpe WH (1963) Learning and instinct in animals. Methuen, London
Tomsic D, de Astrada MB, Sztarker J, Maldonado H (2009) Behavioral and neuronal attributes of short- and long-term habituation in the crab Chasmagnathus. Neurobiol Learn Mem 92:176–182
Trewavas T (2003) Aspects of plant intelligence. Ann Bot 92:1–20
Tseng AS, Levin M (2013) Cracking the bioelectric code: probing endogenous ionic controls of pattern formation. Commun Integr Biol 6:e22595
Turner CH, Robling AG, Duncan RL, Burr DB (2002) Do bone cells behave like a neuronal network? Calcif Tissue Int 70:435–442
Uehlein N, Kaldenhoff R (2008) Aquaporins and plant leaf movements. Ann Bot 101:1–4
Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–1118
Volkov AG, Carrell H, Adesina T, Markin VS, Jovanov E (2008) Plant electrical memory. Plant Signal Behav 3:490–492
Wiel DE, Weeks JC (1996) Habituation and dishabituation of the proleg withdrawal reflex in larvae of the sphinx hawk, Manduca sexta. Behav Neurosci 110:1133–1147
Yaish MW, Colasanti J, Rothstein SJ (2011) The role of epigenetic processes in controlling flowering time in plants exposed to stress. J Exp Bot 62:3727–3735
Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512
Yellen G (1998) The moving parts of voltage-gated ion channels. Q Rev Biophys 31:239–295
Acknowledgments
We thank Elisa Azzarello and Elisa Masi for assistance with setting up the light environments, and Leigh Simmons, Joseph Tomkins, Anthony Trewavas, Daniel Robert for valuable comments on the manuscript. This study was supported by Research Fellowships from the University of Western Australia and the Australian Research Council to M. G. and research funding from European Commission to S. M.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Richard Karban.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gagliano, M., Renton, M., Depczynski, M. et al. Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia 175, 63–72 (2014). https://doi.org/10.1007/s00442-013-2873-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-013-2873-7