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Towards Systemic View for Plant Learning: Ecophysiological Perspective

  • Gustavo M. Souza
  • Gabriel R. A. Toledo
  • Gustavo F. R. Saraiva
Chapter
Part of the Signaling and Communication in Plants book series (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.

References

  1. Abramson CI, Chicas-Mosier AM (2016) Learning in plants: lessons from Mimosa pudica. Front Psychol 7:417PubMedPubMedCentralCrossRefGoogle Scholar
  2. Affifi R (2013) Learning plants: semiosis between the parts and the whole. Biosemiotics 6:547–559CrossRefGoogle Scholar
  3. Agrawal AA (2002) Maternal effects associated with herbivory: mechanisms and consequences of transgenerational induced plant resistance. Ecology 83:3408–3415CrossRefGoogle Scholar
  4. 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 12:135–136PubMedPubMedCentralGoogle Scholar
  5. 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 40:859–863CrossRefGoogle Scholar
  6. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3544PubMedCrossRefGoogle Scholar
  7. Azooz MM, Ahmad P (eds) (2016) Plant-environment interaction. Wiley Blackwell, HobokenGoogle Scholar
  8. Bak P (1996) How nature works. The science of self-organized criticality. Springer, New YorkGoogle Scholar
  9. Balmer A, Pastor V, Gamir J, Flors V, Mauch-Mani B (2015) The ‘prime-ome’: towards a holistic approach to priming. Trends Plant Sci 20:443–452PubMedCrossRefGoogle Scholar
  10. Baluška F (ed) (2013) Long-distance systemic signalling and communication in plants. Springer, BerlinGoogle Scholar
  11. Baluška F, Mancuso S (2007) Plant neurobiology as paradigm shift not only in plant sciences. Plant Signal Behav 2:205–207PubMedPubMedCentralCrossRefGoogle Scholar
  12. Baluška F, Mancuso S, Volkmann D (eds) (2006) Communication in plants: neuronal aspects of plant life. Springer, BerlinGoogle Scholar
  13. Barlow P (2008) Reflections on ‘plant neurobiology’. Biosystems 92:132–147PubMedCrossRefGoogle Scholar
  14. Barlow PW (2010) Plant roots: autopoietic and cognitive constructions. Plant Root 4:40–52CrossRefGoogle Scholar
  15. Bateson G (1972) Steps to an ecology of mind. Jason Aronson Inc., LondonGoogle Scholar
  16. Beggs JM, Plenz D (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23:11167–11177PubMedCrossRefGoogle Scholar
  17. 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 24:5216–5229PubMedCrossRefGoogle Scholar
  18. Bertolli SC, Souza GM (2013) The level of environmental noise affects the physiological performance of Glycine max under water deficit. Theor Exp Plant Physiol 25:36–45CrossRefGoogle Scholar
  19. 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 16:578–585PubMedCrossRefGoogle Scholar
  20. Bolker JA (2000) Modularity in development and why it matters to evo-devo. Am Zool 4:770–776Google Scholar
  21. Brenner ED, Stahlberg R, Mancuso S, Vivanco J, Baluska F, Volkenburgh EV (2006) Plant neurobiology: an integrated view of plant signalling. Trends Plant Sci 11:413–419PubMedPubMedCentralCrossRefGoogle Scholar
  22. Brown RL (2013) Learning, evolvability and exploratory behaviour: extending the evolutionary reach of learning. Biol Philos 28:933–955CrossRefGoogle Scholar
  23. Calvo P (2016) The philosophy of plant neurobiology: a manifesto. Synthese 193:1323–1343CrossRefGoogle Scholar
  24. Camazine S, Deneubourg J-L, Franks NR, Sneyd J, Theraulaz G, Bonabeau E (2001) Self-organization in biological systems. Princeton University Press, Princeton, NJGoogle Scholar
  25. 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 57:2391–2400PubMedCrossRefGoogle Scholar
  26. 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 96:231–236CrossRefGoogle Scholar
  27. Cazalis R, Carletti T, Cottam R (2017) The living organism: strengthening the basis. Biosystems 158:10–16PubMedCrossRefGoogle Scholar
  28. 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 32:2073–2077PubMedCrossRefGoogle Scholar
  29. Choi W, Hilleary R, Swanson SJ, Kim S, Gilroy S (2016) Rapid, long-distance electrical and calcium signalling in plants. Annu Rev Plant Biol 67:287–307PubMedCrossRefGoogle Scholar
  30. Clarke E (2012) Plant individuality: a solution to the demographer’s dilemma. Biol Philos 27:321–361CrossRefGoogle Scholar
  31. 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 19:1062–1071PubMedCrossRefGoogle Scholar
  32. 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:e1501340PubMedPubMedCentralCrossRefGoogle Scholar
  33. 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 116:1351–1357PubMedPubMedCentralCrossRefGoogle Scholar
  34. de Arcangelisa L, Herrmann HJ (2010) Learning as a phenomenon occurring in a critical state. Proc Natl Acad Sci U S A 107:3977–3981CrossRefGoogle Scholar
  35. de Kroon H, Huber H, Stuefer JF, van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82PubMedCrossRefGoogle Scholar
  36. 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 32:704–712PubMedCrossRefGoogle Scholar
  37. De Loof A (2016) The cell’s self-generated “electrome”: the biophysical essence of the immaterial dimension of life? Commun Integr Biol 9:e1197446PubMedPubMedCentralCrossRefGoogle Scholar
  38. Debono MW (2013a) Dynamic protoneural networks in plants: a new approach of spontaneous extracellular potential variations. Plant Signal Behav 8:e24207PubMedPubMedCentralCrossRefGoogle Scholar
  39. Debono MW (2013b) Perceptive levels in plants: a transdisciplinary challenge in living organism’s plasticity. Trans J Eng Sci 4:21–39Google Scholar
  40. DeWitt TJ, Scheiner SM (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, New York, NYGoogle Scholar
  41. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81PubMedCrossRefGoogle Scholar
  42. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785PubMedPubMedCentralCrossRefGoogle Scholar
  43. Eurich CW, Herrmann JM, Ernst UA (2002) Finite-size effects of avalanche dynamics. Phys Rev E 66:066137CrossRefGoogle Scholar
  44. Feyerabend P (1975) Against method. NBL, LondonGoogle Scholar
  45. 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 1–28Google Scholar
  46. Firn R (2004) Plant intelligence: an alternative point of view. Ann Bot 93:345–351PubMedPubMedCentralCrossRefGoogle Scholar
  47. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257PubMedCrossRefGoogle Scholar
  48. 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 10:490–498PubMedCrossRefGoogle Scholar
  49. 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 180:722–734PubMedCrossRefGoogle Scholar
  50. Gagliano M (2015) In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants. AoB Plants 7:plu075CrossRefGoogle Scholar
  51. Gagliano M, Renton M, Depczynski M, Mancuso S (2014) Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia 175:63–72CrossRefPubMedGoogle Scholar
  52. Gagliano M, Vyazovskiy VV, Borbeely AA, Grimonprez M, Depczynski M (2016) Learning by association in plants. Sci Rep 6:38427PubMedPubMedCentralCrossRefGoogle Scholar
  53. Gallé A, Lautner S, Flexas J, Fromm J (2015) Environmental stimuli and physiological responses: the current view on electrical signalling. Env Exp Bot 114:15–21CrossRefGoogle Scholar
  54. Garzón FC (2007) The quest for cognition in plant neurobiology. Plant Signal Behav 2:208–211PubMedPubMedCentralCrossRefGoogle Scholar
  55. Garzón FC, Keijzer F (2011) Plants: adaptive behaviour, root-brains, and minimal cognition. Adapt Behav 19:155–171CrossRefGoogle Scholar
  56. Gibson JJ (1966) The senses considered as perceptual systems. Houghton Mifflin, BostonGoogle Scholar
  57. Gilroy S, Trewavas A (2001) Signal processing and transduction in plant cells: the end of the beginning? Nat Rev Mol Cell Biol 2:307–314PubMedCrossRefGoogle Scholar
  58. 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 36:240–255CrossRefPubMedGoogle Scholar
  59. 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 1–26Google Scholar
  60. Heil M, Kost C (2006) Priming of indirect defences. Ecol Lett 9:813–817PubMedCrossRefGoogle Scholar
  61. 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 104:5467–5472PubMedPubMedCentralCrossRefGoogle Scholar
  62. Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272PubMedCrossRefGoogle Scholar
  63. 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 91:1118–1133PubMedCrossRefGoogle Scholar
  64. 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 114:540–545PubMedCrossRefGoogle Scholar
  65. Holeski LM (2007) Within and among generation phenotypic plasticity in trichrome density of Mimulus guttatus. J Evol Biol 20:2092–2100PubMedCrossRefGoogle Scholar
  66. Holeski LM, Jander G, Agrawal AA (2012) Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol Evol 27(11):618–626PubMedCrossRefGoogle Scholar
  67. Hossain MA, Fujita M (2013) Hydrogen peroxide priming stimulates drought tolerance in mustard (Brassica juncea L.) seedlings. Plant Gene Trait 4:109–123Google Scholar
  68. 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 4:50–70Google Scholar
  69. 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 2:1–14CrossRefGoogle Scholar
  70. 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 6:420PubMedPubMedCentralGoogle Scholar
  71. 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 7:116PubMedPubMedCentralGoogle Scholar
  72. Hütt M-T, Lüttge U (2005) Network dynamics in plant biology: current progress in historical perspective. Prog Bot 66:277–310Google Scholar
  73. 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 30:381–396CrossRefGoogle Scholar
  74. 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 139:267–274PubMedPubMedCentralCrossRefGoogle Scholar
  75. Jenks MA, Hasegawa PM (2014) Plant abiotic stress. Wiley Blackwell, HobokenGoogle Scholar
  76. Jisha KC, Puthur JT (2016) Seed priming with beta-amino butyric acid improves abiotic stress tolerance in rice seedlings. Rice Sci 23:242–254CrossRefGoogle Scholar
  77. Jisha KC, Vijayakumari K, Puthur JT (2013) Seed priming for abiotic stress tolerance: an overview. Acta Physiol Plant 35:1381–1396CrossRefGoogle Scholar
  78. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity RID D-4021-2009. Science 324:89–91PubMedCrossRefGoogle Scholar
  79. Kandel E, Dudai Y, Mayford M (2014) The molecular and systems biology of memory. Cell 157:163–186PubMedCrossRefGoogle Scholar
  80. Karban R (2015) Plant sensing and communication. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  81. 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 148:280–292PubMedCrossRefGoogle Scholar
  82. Kinouchi O, Copelli M (2006) Optimal dynamical range of excitable networks at criticality. Nat Phys 2:348–351CrossRefGoogle Scholar
  83. Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16:681–687PubMedCrossRefGoogle Scholar
  84. 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 128:1046–1056PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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 130:2129–2141PubMedPubMedCentralCrossRefGoogle Scholar
  86. Kron AP, Souza GM, Ribeiro RF (2008) Water deficiency at different developmental stages of glycine max can improve drought tolerance. Bragantia 67:693–699CrossRefGoogle Scholar
  87. Larcher W (1995) Physiological plan ecology, 3rd edn. Springer, BerlinCrossRefGoogle Scholar
  88. 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 26:1176–1185CrossRefGoogle Scholar
  89. Lucas M, Laplaze L, Bennett MJ (2011) Plant systems biology: network matters. Plant Cell Environ 34:535–553PubMedCrossRefGoogle Scholar
  90. Lüttge U (2008) Physiological ecology of tropical plants, 2nd edn. Springer, BerlinGoogle Scholar
  91. Lüttge U (2012) Modularity and emergence: biology’s challenge in understanding life. Plant Biol 14:865–871PubMedCrossRefGoogle Scholar
  92. 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 106:4048–4053PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 136:2818–2830PubMedPubMedCentralCrossRefGoogle Scholar
  94. Maturana HR, Varela FJ (1980) Autopoiesis and cognition: the realization of the leaving. D. Reidel Publishing Company, LondonCrossRefGoogle Scholar
  95. Matyssek R, Lüttge U (2013) Gaia: the Planet Holobiont. Nova Acta Leopold 114:325–344Google Scholar
  96. McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310CrossRefGoogle Scholar
  97. 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 202:499–508PubMedCrossRefGoogle Scholar
  98. Miller JG (1978) Living systems. McGraw-Hill Publishing Co., New YorkGoogle Scholar
  99. Mitchell M (2009) Complexity: a guided tour. Oxford University Press, New YorkGoogle Scholar
  100. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19PubMedCrossRefGoogle Scholar
  101. Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgenerational memory of stress in plants. Nature 442:1046–1049PubMedPubMedCentralCrossRefGoogle Scholar
  102. Møller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution. Oxford University Press, OxfordGoogle Scholar
  103. Mott KA, Buckley TN (2000) Patchy stomatal conductance emergent collective behaviour. Trends Plant Sci 5:258–262PubMedCrossRefGoogle Scholar
  104. 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:e24594PubMedPubMedCentralCrossRefGoogle Scholar
  105. Nicolis G, Prigogine I (1989) Exploring complexity: an introduction. WH Freeman, New YorkGoogle Scholar
  106. Olfati-Saber R, Fax JA, Murray RM (2007) Consensus and cooperation in networked multi-agent systems. Proc IEEE 95:215–233CrossRefGoogle Scholar
  107. 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 34:1281–1293PubMedCrossRefGoogle Scholar
  108. 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 129:460–468PubMedPubMedCentralCrossRefGoogle Scholar
  109. 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 13:276–284PubMedCrossRefGoogle Scholar
  110. 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 161:837–846CrossRefGoogle Scholar
  111. 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 180:511–523PubMedCrossRefGoogle Scholar
  112. Prasch CM, Sonnewald U (2015) Signalling events in plants: stress factors in combination change the picture. Env Exp Bot 114:4–14CrossRefGoogle Scholar
  113. 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 158:854–863PubMedPubMedCentralCrossRefGoogle Scholar
  114. 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 161–188Google Scholar
  115. 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 35:163–175PubMedCrossRefGoogle Scholar
  116. Saraiva GFR, Ferreira AS, Souza GM (2017) Osmotic stress decreases complexity underlying the electrophysiological dynamic in soybean. Plant Biol 19:702–708PubMedCrossRefGoogle Scholar
  117. Schneider ED, Kay JJ (1994) Life as a manifestation of the second law of thermodynamics. Math Comput Model 19:25–48CrossRefGoogle Scholar
  118. Schroeder M (1991) Fractals, Chaos, Power Laws, Minutes From an Infinite Paradise. New York, WH Freeman and CompanyGoogle Scholar
  119. Sheth BP, Thaker VS (2014) Plant systems biology: insights, advances and challenges. Planta 240:33–54PubMedCrossRefGoogle Scholar
  120. Shew WL, Yang H, Petermann T, Roy R, Plenz D (2009) Neuronal avalanches imply maximum dynamic range in cortical networks at criticality. J Neurosci 29:15595–15600PubMedPubMedCentralCrossRefGoogle Scholar
  121. 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 158:835–843PubMedPubMedCentralCrossRefGoogle Scholar
  122. Souza GM, Lüttge U (2015) Stability as a phenomenon emergent from plasticity—complexity—diversity in eco-physiology. Prog Bot 76:211–239Google Scholar
  123. 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 47:423–431Google Scholar
  124. Souza GM, Pincus SM, Monteiro JAF (2005) The complexity-stability hypothesis in plant gas exchange under water deficit. Braz J Plant Physiol 17:363–373CrossRefGoogle Scholar
  125. 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 6:15–26CrossRefGoogle Scholar
  126. 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 77:167–186Google Scholar
  127. Souza GM, Prado CHBA, Ribeiro RV, Barbosa JPRAD, Gonçalves AN, Habermann G (2016b) Toward a systemic plant physiology. Theor Exp Plant Physiol 28:341–346CrossRefGoogle Scholar
  128. 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:e1290040PubMedPubMedCentralCrossRefGoogle Scholar
  129. Sterelny K (2003) Thought in a hostile world: the evolution of human cognition. Wiley-Blackwell, OxfordGoogle Scholar
  130. Struik PC, Yin X, Meinke H (2008) Plant neurobiology and green plant intelligence: science, metaphors and nonsense. J Sci Food Agric 88:363–370CrossRefGoogle Scholar
  131. Sweetlove LJ, Fernie AR (2005) Regulation of metabolic networks: understanding metabolic complexity in the systems biology era. New Phytol 168:9–24PubMedCrossRefGoogle Scholar
  132. Thellier M, Lüttge U (2012) Plant memory: a tentative model. Plant Biol 15:1–12PubMedCrossRefGoogle Scholar
  133. 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 49:16–26PubMedCrossRefGoogle Scholar
  134. Trewavas A (2003) Aspects of plant intelligence. Ann Bot 92:1–20PubMedPubMedCentralCrossRefGoogle Scholar
  135. Trewavas A (2005) Green plants as intelligent organisms. Trends Plant Sci 10:413–419PubMedPubMedCentralCrossRefGoogle Scholar
  136. Trewavas A (2007) Response to Alpi et al.: Plant neurobiology – all metaphors have value. Trends Plant Sci 12:231–233PubMedCrossRefGoogle Scholar
  137. Trewavas A (2009) What is plant behaviour? Plant Cell Environ 32:606–616PubMedCrossRefGoogle Scholar
  138. Trewavas A (2014) Plant behaviour and intelligence. Oxford University Press, OxfordCrossRefGoogle Scholar
  139. 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 9:421–427PubMedCrossRefGoogle Scholar
  140. Van Kleunen M, Fisher M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–56PubMedCrossRefGoogle Scholar
  141. van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448PubMedCrossRefGoogle Scholar
  142. 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 17:895–908CrossRefGoogle Scholar
  143. Verhoeven KJ, van Gurp TP (2012) Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLoS One 7:e38605PubMedPubMedCentralCrossRefGoogle Scholar
  144. 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)PubMedPubMedCentralCrossRefGoogle Scholar
  145. 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 80:54–62CrossRefGoogle Scholar
  146. Von Bertalanffy L (1968) General system theory. George Braziller, New YorkGoogle Scholar
  147. 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 71:34–40CrossRefGoogle Scholar
  148. Watling JR, Robinson SA, Woodrow IE, Osmond CB (1997) Responses of rainforest understorey plants to excess light during sunflecks. Aust J Plant Physiol 24:17–25CrossRefGoogle Scholar
  149. Withagen R, Poel HJ, Araújo D, Pepping G-J (2012) Affordances can invite behavior: reconsidering the relationship between affordances and agency. New Ideas Psychol 30:250–258CrossRefGoogle Scholar
  150. Witzany G (2006) Plant communication from biosemiotic perspective. Plant Signal Behav 1:169–178PubMedPubMedCentralCrossRefGoogle Scholar
  151. Xia JH, Saglio PH (1992) Lactic acid efflux as a mechanism of hypoxic acclimation of maize root tips to anoxia. Plant Physiol 100:40–48PubMedPubMedCentralCrossRefGoogle Scholar
  152. Zheng SJ, Dicke M (2008) Ecological genomics of plant–insect interactions: from gene to community. Plant Physiol 146:812–817PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Gustavo M. Souza
    • 1
  • Gabriel R. A. Toledo
    • 1
  • Gustavo F. R. Saraiva
    • 2
  1. 1.Department of BotanyFederal University of PelotasPelotasBrazil
  2. 2.Research Center for Ecophysiology of West of São PauloSão PauloBrazil

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