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Towards Systemic View for Plant Learning: Ecophysiological Perspective

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Memory and Learning in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Herein, we have proposed a concept of plant learning based on some principles of systemic plant ecophysiology. In order to accomplish this task, a framework consisting in basic epistemological assumptions is offered, as well as a cognitive context that underpins the perspective of learning. Accordingly, a number of empirical studies are quoted to illustrate the basic idea presented herein.

The world is richer than it is possible to express in any single language.

Ilya Prigogine

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References

  • Abramson CI, Chicas-Mosier AM (2016) Learning in plants: lessons from Mimosa pudica. Front Psychol 7:417

    Article  PubMed  PubMed Central  Google Scholar 

  • Affifi R (2013) Learning plants: semiosis between the parts and the whole. Biosemiotics 6:547–559

    Article  Google Scholar 

  • Agrawal AA (2002) Maternal effects associated with herbivory: mechanisms and consequences of transgenerational induced plant resistance. Ecology 83:3408–3415

    Article  Google Scholar 

  • Alpi A, Amrhein N, Bertl A, Blatt MR, Blumwald E, Cervone F, Dainty J, De Michelis MI, Epstein E, Galston AW, Goldsmith MH, Hawes C, Hell R, Hetherington A, Hofte H, Juergens G, Leaver CJ, Moroni A, Murphy A, Oparka K, Perata P, Quader H, Rausch T, Ritzenthaler C, Rivetta A, Robinson DG, Sanders D, Scheres B, Schumacher K, Sentenac H, Slayman CL, Soave C, Somerville C, Taiz L, Thiel G, Wagner R (2007) Plant neurobiology: no brain, no gain? Trends Plant Sci 12:135–136

    CAS  PubMed  Google Scholar 

  • Artetxe U, García-Plazaola JI, Hernández A, Becerril JM (2002) Low light grown duckweed plants are more protected against the toxicity induced by Zn and Cd. Plant Physiol Biochem 40:859–863

    Article  CAS  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3544

    Article  CAS  PubMed  Google Scholar 

  • Azooz MM, Ahmad P (eds) (2016) Plant-environment interaction. Wiley Blackwell, Hoboken

    Google Scholar 

  • Bak P (1996) How nature works. The science of self-organized criticality. Springer, New York

    Google Scholar 

  • Balmer A, Pastor V, Gamir J, Flors V, Mauch-Mani B (2015) The ‘prime-ome’: towards a holistic approach to priming. Trends Plant Sci 20:443–452

    Article  CAS  PubMed  Google Scholar 

  • Baluška F (ed) (2013) Long-distance systemic signalling and communication in plants. Springer, Berlin

    Google Scholar 

  • Baluška F, Mancuso S (2007) Plant neurobiology as paradigm shift not only in plant sciences. Plant Signal Behav 2:205–207

    Article  PubMed  PubMed Central  Google Scholar 

  • Baluška F, Mancuso S, Volkmann D (eds) (2006) Communication in plants: neuronal aspects of plant life. Springer, Berlin

    Google Scholar 

  • Barlow P (2008) Reflections on ‘plant neurobiology’. Biosystems 92:132–147

    Article  PubMed  Google Scholar 

  • Barlow PW (2010) Plant roots: autopoietic and cognitive constructions. Plant Root 4:40–52

    Article  Google Scholar 

  • Bateson G (1972) Steps to an ecology of mind. Jason Aronson Inc., London

    Google Scholar 

  • Beggs JM, Plenz D (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23:11167–11177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beggs JM, Plenz D (2004) Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J Neurosci 24:5216–5229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertolli SC, Souza GM (2013) The level of environmental noise affects the physiological performance of Glycine max under water deficit. Theor Exp Plant Physiol 25:36–45

    Article  CAS  Google Scholar 

  • Bertolli SC, Mazzafera P, Souza GM (2014) Why is it so difficult to identify a single indicator of water stress in plants? A proposal for a multivariate analysis to assess emergent properties. Plant Biol 16:578–585

    Article  CAS  PubMed  Google Scholar 

  • Bolker JA (2000) Modularity in development and why it matters to evo-devo. Am Zool 4:770–776

    Google Scholar 

  • Brenner ED, Stahlberg R, Mancuso S, Vivanco J, Baluska F, Volkenburgh EV (2006) Plant neurobiology: an integrated view of plant signalling. Trends Plant Sci 11:413–419

    Article  CAS  PubMed  Google Scholar 

  • Brown RL (2013) Learning, evolvability and exploratory behaviour: extending the evolutionary reach of learning. Biol Philos 28:933–955

    Article  Google Scholar 

  • Calvo P (2016) The philosophy of plant neurobiology: a manifesto. Synthese 193:1323–1343

    Article  Google Scholar 

  • Camazine S, Deneubourg J-L, Franks NR, Sneyd J, Theraulaz G, Bonabeau E (2001) Self-organization in biological systems. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Capiati DA, País SM, Téllez-Iñón MT (2006) Wounding increases salt tolerance in tomato plants: evidence on the participation of calmodulin-like activities in cross-tolerance signalling. J Exp Bot 57:2391–2400

    Article  CAS  PubMed  Google Scholar 

  • Cayuela E, Perez-Alfocea K, Caro M, Bolarin MC (1996) Priming of seeds with NaCl induces physiological changes in tomato plants grown under salt stress. Physiol Plant 96:231–236

    Article  CAS  Google Scholar 

  • Cazalis R, Carletti T, Cottam R (2017) The living organism: strengthening the basis. Biosystems 158:10–16

    Article  PubMed  Google Scholar 

  • Choh Y, Takabayashi J (2006) Herbivore-induced extrafloral nectar production in lima bean plants enhanced by previous exposure to volatiles from infested conspecifics. J Chem Ecol 32:2073–2077

    Article  CAS  PubMed  Google Scholar 

  • Choi W, Hilleary R, Swanson SJ, Kim S, Gilroy S (2016) Rapid, long-distance electrical and calcium signalling in plants. Annu Rev Plant Biol 67:287–307

    Article  CAS  PubMed  Google Scholar 

  • Clarke E (2012) Plant individuality: a solution to the demographer’s dilemma. Biol Philos 27:321–361

    Article  Google Scholar 

  • Conrath U, Beckers GJ, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant-Microbe Interact 19:1062–1071

    Article  CAS  PubMed  Google Scholar 

  • Crisp PA, Ganguly D, Eichten SE, Borevitz JO, Pogson BJ (2016) Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2:e1501340

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Arcangelisa L, Herrmann HJ (2010) Learning as a phenomenon occurring in a critical state. Proc Natl Acad Sci U S A 107:3977–3981

    Article  Google Scholar 

  • de Kroon H, Huber H, Stuefer JF, van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82

    Article  PubMed  Google Scholar 

  • de Kroon H, Visser EJW, Huber H, Mommer L, Hutchings MJ (2009) A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant Cell Environ 32:704–712

    Article  PubMed  CAS  Google Scholar 

  • De Loof A (2016) The cell’s self-generated “electrome”: the biophysical essence of the immaterial dimension of life? Commun Integr Biol 9:e1197446

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Debono MW (2013a) Dynamic protoneural networks in plants: a new approach of spontaneous extracellular potential variations. Plant Signal Behav 8:e24207

    Article  PubMed  PubMed Central  Google Scholar 

  • Debono MW (2013b) Perceptive levels in plants: a transdisciplinary challenge in living organism’s plasticity. Trans J Eng Sci 4:21–39

    Google Scholar 

  • DeWitt TJ, Scheiner SM (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, New York, NY

    Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  CAS  PubMed  Google Scholar 

  • Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eurich CW, Herrmann JM, Ernst UA (2002) Finite-size effects of avalanche dynamics. Phys Rev E 66:066137

    Article  CAS  Google Scholar 

  • Feyerabend P (1975) Against method. NBL, London

    Google Scholar 

  • Filippou P, Tanou G, Molassiotis A, Fotopoulos V (2012) Plant acclimation to environmental stress using priming agents. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Berlin, NY, Springer Science & Business Media, pp 1–28

    Google Scholar 

  • Firn R (2004) Plant intelligence: an alternative point of view. Ann Bot 93:345–351

    Article  PubMed  PubMed Central  Google Scholar 

  • Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257

    Article  CAS  PubMed  Google Scholar 

  • Frost CJ, Heidi MA, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes response against herbivores. Ecol Lett 10:490–498

    Article  PubMed  Google Scholar 

  • Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180:722–734

    Article  CAS  PubMed  Google Scholar 

  • Gagliano M (2015) In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants. AoB Plants 7:plu075

    Article  Google Scholar 

  • Gagliano M, Renton M, Depczynski M, Mancuso S (2014) Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia 175:63–72

    Article  PubMed  Google Scholar 

  • Gagliano M, Vyazovskiy VV, Borbeely AA, Grimonprez M, Depczynski M (2016) Learning by association in plants. Sci Rep 6:38427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallé A, Lautner S, Flexas J, Fromm J (2015) Environmental stimuli and physiological responses: the current view on electrical signalling. Env Exp Bot 114:15–21

    Article  Google Scholar 

  • Garzón FC (2007) The quest for cognition in plant neurobiology. Plant Signal Behav 2:208–211

    Article  PubMed  PubMed Central  Google Scholar 

  • Garzón FC, Keijzer F (2011) Plants: adaptive behaviour, root-brains, and minimal cognition. Adapt Behav 19:155–171

    Article  Google Scholar 

  • Gibson JJ (1966) The senses considered as perceptual systems. Houghton Mifflin, Boston

    Google Scholar 

  • Gilroy S, Trewavas A (2001) Signal processing and transduction in plant cells: the end of the beginning? Nat Rev Mol Cell Biol 2:307–314

    Article  CAS  PubMed  Google Scholar 

  • Goh CH, Gil Nam H, Shin Park Y (2003) Stress memory in plants: a negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants. Plant J 36:240–255

    Article  CAS  PubMed  Google Scholar 

  • Gomila T, Calvo P (2008) Directions for an embodied cognitive science: toward an integrated approach. In: Calvo P, Gomila T (eds) Handbook of cognitive science: an embodied approach. Elsevier, San Diego, pp 1–26

    Google Scholar 

  • Heil M, Kost C (2006) Priming of indirect defences. Ecol Lett 9:813–817

    Article  PubMed  Google Scholar 

  • Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci U S A 104:5467–5472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272

    Article  CAS  PubMed  Google Scholar 

  • Hilker M, Schwachtje J, Baier M, Balazadeh S, Bäurle I, Geiselhardt S, Hincha DK, Kunze R, Mueller-Roeber B, Rillig MC, Rolff J, Romeis T, Schmülling T, Steppuhn A, van Dongen J, Whitcomb SJ, Wurst S, Zuther E, Kopka J (2016) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev Camb Philos Soc 91:1118–1133

    Article  PubMed  Google Scholar 

  • Hirao T, Okazawa A, Harada K, Kobayashi A, Muranaka T, Kirata K (2012) Green leaf volatiles enhance methyl jasmonate response in Arabidopsis. J Biosci Bioeng 114:540–545

    Article  CAS  PubMed  Google Scholar 

  • Holeski LM (2007) Within and among generation phenotypic plasticity in trichrome density of Mimulus guttatus. J Evol Biol 20:2092–2100

    Article  CAS  PubMed  Google Scholar 

  • Holeski LM, Jander G, Agrawal AA (2012) Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol Evol 27(11):618–626

    Article  PubMed  Google Scholar 

  • Hossain MA, Fujita M (2013) Hydrogen peroxide priming stimulates drought tolerance in mustard (Brassica juncea L.) seedlings. Plant Gene Trait 4:109–123

    Google Scholar 

  • Hossain MA, Mostofa MG, Fujita M (2013a) Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol Plant Breed 4:50–70

    Google Scholar 

  • Hossain MA, Mostofa MG, Fujita M (2013b) Heat-shock positively modulates oxidative protection of salt and drought-stressed mustard (Brassica campestris L.) seedlings. J Plant Sci Mol Breed 2:1–14

    Article  CAS  Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, Burritt DJ, Fujita M, Tran LS (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420

    PubMed  PubMed Central  Google Scholar 

  • Hussain S, Khan F, Hussain HA, Nie L (2016) Physiological and biochemical mechanisms of seed priming-induced chilling tolerance in rice cultivars. Front Plant Sci 7:116

    PubMed  PubMed Central  Google Scholar 

  • Hütt M-T, Lüttge U (2005) Network dynamics in plant biology: current progress in historical perspective. Prog Bot 66:277–310

    Google Scholar 

  • Iqbal M, Ashraf M (2007) Seed preconditioning modulates growth, ionic relations, and photosynthetic capacity in adult plants of hexaploid wheat under salt stress. J Plant Nutr 30:381–396

    Article  CAS  Google Scholar 

  • Jakab G, Ton J, Flors V, Zimmerli L, Métraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenks MA, Hasegawa PM (2014) Plant abiotic stress. Wiley Blackwell, Hoboken

    Google Scholar 

  • Jisha KC, Puthur JT (2016) Seed priming with beta-amino butyric acid improves abiotic stress tolerance in rice seedlings. Rice Sci 23:242–254

    Article  Google Scholar 

  • Jisha KC, Vijayakumari K, Puthur JT (2013) Seed priming for abiotic stress tolerance: an overview. Acta Physiol Plant 35:1381–1396

    Article  Google Scholar 

  • Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity RID D-4021-2009. Science 324:89–91

    Article  PubMed  CAS  Google Scholar 

  • Kandel E, Dudai Y, Mayford M (2014) The molecular and systems biology of memory. Cell 157:163–186

    Article  CAS  PubMed  Google Scholar 

  • Karban R (2015) Plant sensing and communication. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292

    Article  PubMed  Google Scholar 

  • Kinouchi O, Copelli M (2006) Optimal dynamical range of excitable networks at criticality. Nat Phys 2:348–351

    Article  CAS  Google Scholar 

  • Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16:681–687

    Article  CAS  PubMed  Google Scholar 

  • Kohler A, Schwindling S, Conrath U (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128:1046–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kron AP, Souza GM, Ribeiro RF (2008) Water deficiency at different developmental stages of glycine max can improve drought tolerance. Bragantia 67:693–699

    Article  Google Scholar 

  • Larcher W (1995) Physiological plan ecology, 3rd edn. Springer, Berlin

    Book  Google Scholar 

  • Li T, Holopainen JK, Kokko H, Tervahauta AI, Blande JD (2012) Herbivore-induced aspen volatiles temporally regulate two different indirect defences in neighbouring plants. Funct Ecol 26:1176–1185

    Article  Google Scholar 

  • Lucas M, Laplaze L, Bennett MJ (2011) Plant systems biology: network matters. Plant Cell Environ 34:535–553

    Article  PubMed  Google Scholar 

  • Lüttge U (2008) Physiological ecology of tropical plants, 2nd edn. Springer, Berlin

    Google Scholar 

  • Lüttge U (2012) Modularity and emergence: biology’s challenge in understanding life. Plant Biol 14:865–871

    Article  PubMed  Google Scholar 

  • Masi E, Ciszak M, Stefano G, Renna L, Azzarello E, Pandolfi C, Mugnai S, Baluska F, Arecchi FT, Mancuso S (2009) Spatiotemporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci U S A 106:4048–4053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mateo A, Mühlenbock P, Rustérucci C, Chang CC, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maturana HR, Varela FJ (1980) Autopoiesis and cognition: the realization of the leaving. D. Reidel Publishing Company, London

    Book  Google Scholar 

  • Matyssek R, Lüttge U (2013) Gaia: the Planet Holobiont. Nova Acta Leopold 114:325–344

    Google Scholar 

  • McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310

    Article  CAS  Google Scholar 

  • Merilo E, Jõesaar I, Brosché M, Kollist H (2014) To open or to close: species-specific stomatal responses to simultaneously applied opposing environmental factors. New Phytol 202:499–508

    Article  PubMed  Google Scholar 

  • Miller JG (1978) Living systems. McGraw-Hill Publishing Co., New York

    Google Scholar 

  • Mitchell M (2009) Complexity: a guided tour. Oxford University Press, New York

    Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  PubMed  Google Scholar 

  • Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgenerational memory of stress in plants. Nature 442:1046–1049

    Article  CAS  PubMed  Google Scholar 

  • Møller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Mott KA, Buckley TN (2000) Patchy stomatal conductance emergent collective behaviour. Trends Plant Sci 5:258–262

    Article  CAS  PubMed  Google Scholar 

  • Muroi A, Ramadan A, Nishihara M, Yamamoto M, Ozawa R, Takabayashi J, Arimura G (2011) The composite effect of transgenic plant volatiles for acquired immunity to herbivory caused by inter-plant communications. PLoS One 6:e24594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicolis G, Prigogine I (1989) Exploring complexity: an introduction. WH Freeman, New York

    Google Scholar 

  • Olfati-Saber R, Fax JA, Murray RM (2007) Consensus and cooperation in networked multi-agent systems. Proc IEEE 95:215–233

    Article  Google Scholar 

  • Paparella S, Araújo SS, Rossi G, Wijayasinghe M, Carbonera D, Balestrazzi A (2015) Seed priming: state of the art and new perspectives. Plant Cell Rep 34:1281–1293

    Article  CAS  PubMed  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129:460–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng J, van Loon JJA, Zheng S, Dicke M (2011) Herbivore-induced volatiles of cabbage (Brassica oleracea) prime defense responses in neighboring intact plants. Plant Biol 13:276–284

    Article  CAS  PubMed  Google Scholar 

  • Peñuelas J, Filella I, Zhang X, Llorens L, Ogaya R, Lloret R, Comas P, Estiarte M, Terradas J (2004) Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol 161:837–846

    Article  PubMed  Google Scholar 

  • Pozo MJ, Van Der Ent S, Van Loon LC, Pieterse CMJ (2008) Transcription factor MYC2 is involved in priming for enhanced defence during rhizobacteria-induced systemic resistance in Arabidopsis thaliana RID A-9326-2011. New Phytol 180:511–523

    Article  CAS  PubMed  Google Scholar 

  • Prasch CM, Sonnewald U (2015) Signalling events in plants: stress factors in combination change the picture. Env Exp Bot 114:4–14

    Article  CAS  Google Scholar 

  • Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158:854–863

    Article  CAS  PubMed  Google Scholar 

  • Richardson MJ, Shockley K, Fajen BR, Riley MA, Turvey MT (2008) Ecological psychology: six principles for an embodied–embedded approach to behaviour. In: Calvo P, Gomila T (eds) Handbook of cognitive science: an embodied approach. Elsevier, San Diego, pp 161–188

    Google Scholar 

  • Rodriguez-Saona CR, Rodriguez-Saona LE, Frost CJ (2009) Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol 35:163–175

    Article  CAS  PubMed  Google Scholar 

  • Saraiva GFR, Ferreira AS, Souza GM (2017) Osmotic stress decreases complexity underlying the electrophysiological dynamic in soybean. Plant Biol 19:702–708

    Article  CAS  PubMed  Google Scholar 

  • Schneider ED, Kay JJ (1994) Life as a manifestation of the second law of thermodynamics. Math Comput Model 19:25–48

    Article  Google Scholar 

  • Schroeder M (1991) Fractals, Chaos, Power Laws, Minutes From an Infinite Paradise. New York, WH Freeman and Company

    Google Scholar 

  • Sheth BP, Thaker VS (2014) Plant systems biology: insights, advances and challenges. Planta 240:33–54

    Article  CAS  PubMed  Google Scholar 

  • Shew WL, Yang H, Petermann T, Roy R, Plenz D (2009) Neuronal avalanches imply maximum dynamic range in cortical networks at criticality. J Neurosci 29:15595–15600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slaughter A, Daniel X, Flors V, Luna E, Hohn E, Mauch-Mani B (2012) Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:835–843

    Article  CAS  PubMed  Google Scholar 

  • Souza GM, Lüttge U (2015) Stability as a phenomenon emergent from plasticity—complexity—diversity in eco-physiology. Prog Bot 76:211–239

    Google Scholar 

  • Souza GM, de Oliveira RF, Cardoso VJM (2004) Temporal dynamics of stomatal conductance of plants under water deficit: can homeostasis be improved by more complex dynamics. Arq Biol Tecnol Curitiba 47:423–431

    Google Scholar 

  • Souza GM, Pincus SM, Monteiro JAF (2005) The complexity-stability hypothesis in plant gas exchange under water deficit. Braz J Plant Physiol 17:363–373

    Article  CAS  Google Scholar 

  • Souza GM, Ribeiro RV, Prado CHBS, Damineli DSC, Sato AM, Oliveira MS (2009) Using network connectance and autonomy analyses to uncover patterns of photosynthetic responses in tropical woody species. Ecol Complex 6:15–26

    Article  Google Scholar 

  • Souza GM, Bertolli SC, Lüttge U (2016a) Hierarchy and information in a system approach to plant biology: explaining the irreducibility in plant ecophysiology. Progr Bot 77:167–186

    Google Scholar 

  • Souza GM, Prado CHBA, Ribeiro RV, Barbosa JPRAD, Gonçalves AN, Habermann G (2016b) Toward a systemic plant physiology. Theor Exp Plant Physiol 28:341–346

    Article  CAS  Google Scholar 

  • Souza GM, Ferreira AS, Saraiva GFR, Toledo GRA (2017) Plant “electrome” can be pushed toward a self-organized critical state by external cues: evidences from a study with soybean seedlings subject to different environmental conditions. Plant Signal Behav 12:e1290040

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sterelny K (2003) Thought in a hostile world: the evolution of human cognition. Wiley-Blackwell, Oxford

    Google Scholar 

  • Struik PC, Yin X, Meinke H (2008) Plant neurobiology and green plant intelligence: science, metaphors and nonsense. J Sci Food Agric 88:363–370

    Article  CAS  Google Scholar 

  • Sweetlove LJ, Fernie AR (2005) Regulation of metabolic networks: understanding metabolic complexity in the systems biology era. New Phytol 168:9–24

    Article  CAS  PubMed  Google Scholar 

  • Thellier M, Lüttge U (2012) Plant memory: a tentative model. Plant Biol 15:1–12

    Article  PubMed  CAS  Google Scholar 

  • Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TC (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26

    Article  CAS  PubMed  Google Scholar 

  • Trewavas A (2003) Aspects of plant intelligence. Ann Bot 92:1–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trewavas A (2005) Green plants as intelligent organisms. Trends Plant Sci 10:413–419

    Article  CAS  PubMed  Google Scholar 

  • Trewavas A (2007) Response to Alpi et al.: Plant neurobiology – all metaphors have value. Trends Plant Sci 12:231–233

    Article  CAS  PubMed  Google Scholar 

  • Trewavas A (2009) What is plant behaviour? Plant Cell Environ 32:606–616

    Article  PubMed  Google Scholar 

  • Trewavas A (2014) Plant behaviour and intelligence. Oxford University Press, Oxford

    Book  Google Scholar 

  • Turlings TCJ, Ton J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opin Plant Biol 9:421–427

    Article  PubMed  Google Scholar 

  • Van Kleunen M, Fisher M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–56

    Article  PubMed  Google Scholar 

  • van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  PubMed  CAS  Google Scholar 

  • Verhagen BW, Glazebrook J, Zhu T, Chang HS, van Loon LC, Pieterse CM (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant Microb Interact 17:895–908

    Article  CAS  Google Scholar 

  • Verhoeven KJ, van Gurp TP (2012) Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLoS One 7:e38605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vialet-Chabrand S, Matthews JSA, Simkin AJ, Raines CA, Lawson T (2017) Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiol 173(4):2163–2179 (in press)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vítolo HF, Souza GM, Silveira JAG (2012) Cross-scale multivariate analysis of physiological responses to high temperature in two tropical crops with C3 and C4 metabolism. Env Exp Bot 80:54–62

    Article  CAS  Google Scholar 

  • Von Bertalanffy L (1968) General system theory. George Braziller, New York

    Google Scholar 

  • Walter J, Nagy L, Heinb R, Rascher U, Beierkuhnleinb C, Willner E, Jentsch A (2011) Do plants remember drought? Hints towards a drought-memory in grasses. Environ Exp Bot 71:34–40

    Article  Google Scholar 

  • Watling JR, Robinson SA, Woodrow IE, Osmond CB (1997) Responses of rainforest understorey plants to excess light during sunflecks. Aust J Plant Physiol 24:17–25

    Article  Google Scholar 

  • Withagen R, Poel HJ, Araújo D, Pepping G-J (2012) Affordances can invite behavior: reconsidering the relationship between affordances and agency. New Ideas Psychol 30:250–258

    Article  Google Scholar 

  • Witzany G (2006) Plant communication from biosemiotic perspective. Plant Signal Behav 1:169–178

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia JH, Saglio PH (1992) Lactic acid efflux as a mechanism of hypoxic acclimation of maize root tips to anoxia. Plant Physiol 100:40–48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng SJ, Dicke M (2008) Ecological genomics of plant–insect interactions: from gene to community. Plant Physiol 146:812–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Botany, Federal University of Pelotas, Pelotas, Brazil

    Gustavo M. Souza & Gabriel R. A. Toledo

  2. Research Center for Ecophysiology of West of São Paulo, São Paulo, Brazil

    Gustavo F. R. Saraiva

Authors
  1. Gustavo M. Souza
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  2. Gabriel R. A. Toledo
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  3. Gustavo F. R. Saraiva
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Corresponding author

Correspondence to Gustavo M. Souza .

Editor information

Editors and Affiliations

  1. Department of Plant Cell Biology, IZMB, University of Bonn, Bonn, Germany

    Frantisek Baluska

  2. School of Animal Biology, University of Western Australia, Crawley, Western Autralia, Australia

    Monica Gagliano

  3. Telos- Philosophische Praxis, Buermoos, Salzburg, Austria

    Guenther Witzany

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Souza, G.M., Toledo, G.R.A., Saraiva, G.F.R. (2018). Towards Systemic View for Plant Learning: Ecophysiological Perspective. In: Baluska, F., Gagliano, M., Witzany, G. (eds) Memory and Learning in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-75596-0_9

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