A roadmap towards a functional paradigm for learning & memory in plants.

In plants, the acquisition, processing and storage of empirical information can result in the modification of their behavior according to the nature of the stimulus, and yet this area of research remained relatively understudied until recently. As the body of evidence supporting the inclusion of plants among the higher organisms demonstrating the adaptations to accomplish these tasks keeps increasing, the resistance by traditional botanists and agricultural scientists, who were at first cautious in allowing the application of animal models onto plant physiology and development, subsides. However, the debate retains much of its heat, a good part of it originating from the controversial use of nervous system terms to describe plant processes. By focusing on the latest findings on the cellular and molecular mechanisms underlying the well established processes of Learning and Memory, recognizing what has been accomplished and what remains to be explored, and without seeking to bootstrap neuronal characteristics where none are to be found, a roadmap guiding towards a comprehensive paradigm for Learning and Memory in plants begins to emerge. Meanwhile the applications of the new field of Plant Gnosophysiology look as promising as ever.

[1]  Richard Karban,et al.  Seasonal variation of responses to herbivory and volatile communication in sagebrush (Artemisia tridentata) (Asteraceae) , 2016, Journal of Plant Research.

[2]  John C. Walker,et al.  Plant Protein Kinase Families and Signal Transduction , 1995, Plant physiology.

[3]  Stefan Mayr,et al.  Ultrasonic emissions during ice nucleation and propagation in plant xylem , 2015, The New phytologist.

[4]  M. Evans,et al.  Correlations between gravitropic curvature and auxin movement across gravistimulated roots of Zea mays. , 1990, Plant physiology.

[5]  David Johnson,et al.  Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. , 2013, Ecology letters.

[6]  Geoffrey G. Parker,et al.  Mechanical abrasion and intercrown spacing , 1984 .

[7]  Ottoline Leyser,et al.  The control of shoot branching: an example of plant information processing. , 2009, Plant, cell & environment.

[8]  Julian I Schroeder,et al.  Reactive Oxygen Species Activation of Plant Ca2+ Channels. A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechanotransduction1 , 2004, Plant Physiology.

[9]  Kevin M Manz,et al.  A novel adolescent chronic social defeat model: reverse-Resident-Intruder Paradigm (rRIP) in male rats , 2018, Stress.

[10]  E. Nishida,et al.  The MAP kinase cascade is essential for diverse signal transduction pathways. , 1993, Trends in biochemical sciences.

[11]  E R Kandel,et al.  A Direct Synaptic Connection Mediating Both Excitation and Inhibition , 1967, Science.

[12]  Chandra L Tucker,et al.  Light-dependent, Dark-promoted Interaction between Arabidopsis Cryptochrome 1 and Phytochrome B Proteins*♦ , 2012, The Journal of Biological Chemistry.

[13]  Richard Karban,et al.  Volatile communication between plants that affects herbivory: a meta-analysis. , 2014, Ecology letters.

[14]  Patrick Favre,et al.  Voltage-dependent action potentials in Arabidopsis thaliana. , 2007, Physiologia plantarum.

[15]  Narendra Tuteja,et al.  Calcium Signaling Network in Plants , 2007, Plant signaling & behavior.

[16]  P. Zambryski,et al.  Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. , 2000, Annual review of cell and developmental biology.

[17]  Silvia B. Kikuta,et al.  Ultrasound acoustic emissions from freezing xylem , 2003 .

[18]  Simon J Elsässer,et al.  Evolution of epigenetic chromatin states. , 2017, Current opinion in chemical biology.

[19]  Karl J. Friston,et al.  Predicting green: really radical (plant) predictive processing , 2017, Journal of The Royal Society Interface.

[20]  M. Renton,et al.  Experience teaches plants to learn faster and forget slower in environments where it matters , 2014, Oecologia.

[21]  A. Volkov,et al.  Plant Electrophysiology : Signaling and Responses , 2012 .

[22]  J. S. Lee,et al.  Competitive binding of antagonistic peptides fine-tunes stomatal patterning , 2015, Nature.

[23]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[24]  N. Brereton,et al.  Trees, fungi and bacteria: tripartite metatranscriptomics of a root microbiome responding to soil contamination , 2018, Microbiome.

[25]  D. Shohamy,et al.  A Role for the Medial Temporal Lobe in Feedback-Driven Learning: Evidence from Amnesia , 2013, The Journal of Neuroscience.

[26]  Hatsuo Hayashi,et al.  Stochastic resonance in the hippocampal CA3-CA1 model: a possible memory recall mechanism , 2002, Neural Networks.

[27]  Ramanjulu Sunkar,et al.  Gene regulation during cold stress acclimation in plants. , 2010, Methods in molecular biology.

[28]  H. Appel,et al.  Plants respond to leaf vibrations caused by insect herbivore chewing , 2014, Oecologia.

[29]  G. Laue,et al.  Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush , 2000, Oecologia.

[30]  A. D. Hershey,et al.  INDEPENDENT FUNCTIONS OF VIRAL PROTEIN AND NUCLEIC ACID IN GROWTH OF BACTERIOPHAGE , 1952, The Journal of general physiology.

[31]  Abdul Ahad Buhroo,et al.  Mechanisms of plant defense against insect herbivores , 2012, Plant signaling & behavior.

[32]  C. H. Bailey,et al.  The anatomy of a memory: convergence of results across a diversity of tests , 1988, Trends in Neurosciences.

[33]  G. Hagen,et al.  Auxin signal transduction. , 2015, Essays in biochemistry.

[34]  Tiina Viita,et al.  From Cytoskeleton to Gene Expression: Actin in the Nucleus. , 2016, Handbook of experimental pharmacology.

[35]  C. Staiger,et al.  The role of the actin cytoskeleton in plant cell signaling. , 2004, The New phytologist.

[36]  Cindy Martens,et al.  Methylome and Epialleles in Rice Epilines Selected for Energy Use Efficiency , 2018, Agronomy.

[37]  P. Gruba,et al.  Inter-crown versus under-crown area: contribution of local configuration of trees to variation in topsoil morphology, pH and moisture in Abies alba Mill. forests , 2011, European Journal of Forest Research.

[38]  I. Baldwin,et al.  Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata , 2006, Oecologia.

[39]  R. Hangarter,et al.  Phototropism: Bending towards Enlightenment , 2006, The Plant Cell Online.

[40]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

[41]  Susan A Dudley,et al.  Kin recognition in an annual plant , 2007, Biology Letters.

[42]  Ottoline Leyser,et al.  Ubiquitination and auxin signaling: a degrading story. , 2002, The Plant cell.

[43]  P. Benfey,et al.  Information processing without brains – the power of intercellular regulators in plants , 2010, Development.

[44]  Keara A Franklin,et al.  Photoreceptor crosstalk in shade avoidance. , 2016, Current opinion in plant biology.

[45]  Jiří Friml,et al.  Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis , 2011, Nature Cell Biology.

[46]  A. Kacelnik,et al.  Pea Plants Show Risk Sensitivity , 2016, Current Biology.

[47]  Pierre Bonnet,et al.  Intercellular communication in plants: evidence for two rapidly transmitted systemic signals generated in response to electromagnetic field stimulation in tomato. , 2007, Plant, cell & environment.

[48]  Chris Hawes,et al.  Plant neurobiology: no brain, no gain? , 2007, Trends in plant science.

[49]  N V Raikhel,et al.  Signal transduction networks and the biology of plant cells. , 1999, Biological research.

[50]  Young-Min Woo,et al.  PLASMODESMATA AND CELL-TO-CELL COMMUNICATION IN PLANTS , 1999 .

[51]  František Baluška,et al.  Microorganism and filamentous fungi drive evolution of plant synapses , 2013, Front. Cell. Infect. Microbiol..

[52]  S. Laurence,et al.  The ontology of concepts: Abstract objects or mental representations? , 2007 .

[53]  Anthony Trewavas,et al.  Aspects of plant intelligence. , 2003, Annals of botany.

[54]  Giorgio Grasselli,et al.  Calcium threshold shift enables frequency-independent control of plasticity by an instructive signal , 2016, Proceedings of the National Academy of Sciences.

[55]  J. Fromm,et al.  Electrical signals and their physiological significance in plants. , 2007, Plant, cell & environment.

[56]  David W. Nauen,et al.  Coactivation and timing-dependent integration of synaptic potentiation and depression , 2005, Nature Neuroscience.

[57]  Annika E Huber,et al.  Long-distance plant signaling pathways in response to multiple stressors: the gap in knowledge. , 2016, Journal of experimental botany.

[58]  Sir Thomas Browne The Garden of Cyrus , 2020 .

[59]  H. Bais,et al.  Root exudates mediate kin recognition in plants , 2010, Communicative & integrative biology.

[60]  Stefano Mancuso,et al.  Acoustic and magnetic communication in plants , 2012, Plant signaling & behavior.

[61]  N. A. Walker,et al.  Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata , 2000, Planta.

[62]  Stefano Mancuso,et al.  Plant neurobiology: an integrated view of plant signaling. , 2006, Trends in plant science.

[63]  P. Bonfante,et al.  Plants, Mycorrhizal Fungi and Endobacteria: a Dialog Among Cells and Genomes , 2003, The Biological Bulletin.

[64]  K. Donohue,et al.  DENSITY-DEPENDENT MULTILEVEL SELECTION IN THE GREAT LAKES SEA ROCKET , 2004 .

[65]  J. Wilson,et al.  Phototropic auxin redistribution in corn coleoptiles. , 1957, Science.

[66]  G. Muday,et al.  Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. , 2000, Plant physiology.

[67]  Y. Fukano,et al.  Self-discrimination in the tendrils of the vine Cayratia japonica is mediated by physiological connection , 2015, Proceedings of the Royal Society B: Biological Sciences.

[68]  G. Augustine,et al.  Local Calcium Signaling in Neurons , 2003, Neuron.

[69]  Raphael Lamprecht,et al.  The Role of Actin Cytoskeleton in Dendritic Spines in the Maintenance of Long-Term Memory , 2018, Front. Mol. Neurosci..

[70]  Dhinesh Kumar,et al.  Transcription factor-mediated cell-to-cell signalling in plants. , 2014, Journal of experimental botany.

[71]  Lila Davachi,et al.  Behavioral / Systems / Cognitive Differential Encoding Mechanisms for Subsequent Associative Recognition and Free Recall , 2012 .

[72]  Christina L. Williams,et al.  The Cholinergic System Modulates Memory and Hippocampal Plasticity via Its Interactions with Non-Neuronal Cells , 2017, Front. Immunol..

[73]  Ted C. J. Turlings,et al.  Indole is an essential herbivore-induced volatile priming signal in maize , 2015, Nature Communications.

[74]  Kees van Oers,et al.  Phenology, seasonal timing and circannual rhythms: towards a unified framework , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[75]  Dimitrios Michmizos,et al.  Synaptic Plasticity: A Unifying Model to Address Some Persisting Questions , 2011, The International journal of neuroscience.

[76]  J. J. Camacho-Cristóbal,et al.  Transcription factors as potential participants in the signal transduction pathway of boron deficiency , 2013, Plant signaling & behavior.

[77]  C. Dumas,et al.  First evidence of a calcium transient in flowering plants at fertilization. , 1997, Development.

[78]  M. Netea,et al.  Trained immunity: a memory for innate host defense. , 2011, Cell host & microbe.

[79]  Michael Hollmann,et al.  Arabidopsis thaliana glutamate receptor ion channel function demonstrated by ion pore transplantation. , 2008, Journal of molecular biology.

[80]  W. Briggs,et al.  Photoreceptors in plant photomorphogenesis to date. Five phytochromes, two cryptochromes, one phototropin, and one superchrome. , 2001, Plant physiology.

[81]  C. Wasternack,et al.  Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. , 2007, Annals of botany.

[82]  Etsuro Ito,et al.  Long-term potentiation in the optic tectum of rainbow trout , 2004, Neuroscience Letters.

[83]  J. Kipnis,et al.  Learning and memory … and the immune system , 2013, Learning & memory.

[84]  E. Blancaflor,et al.  Regulation of plant gravity sensing and signaling by the actin cytoskeleton. , 2013, American journal of botany.

[85]  Emmanuel Liscum,et al.  Phototropism: Growing towards an Understanding of Plant Movement[OPEN] , 2014, Plant Cell.

[86]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[87]  Wittko Francke,et al.  Identification of an insect-produced olfactory cue that primes plant defenses , 2017, Nature Communications.

[88]  B. Ding,et al.  Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll , 1996 .

[89]  Blake W. Johnson,et al.  Long‐term potentiation of human visual evoked responses , 2005, The European journal of neuroscience.

[90]  Anna Dzier y ska,et al.  The role of cytoskeleton in stomata functioning , 2006, Acta Physiologiae Plantarum.

[91]  Daniel H Mathalon,et al.  Long-term potentiation (LTP) of human sensory-evoked potentials. , 2010, Wiley interdisciplinary reviews. Cognitive science.

[92]  Frantisek Baluska,et al.  Plant synapses: actin-based domains for cell-to-cell communication. , 2005, Trends in plant science.

[93]  Sergey Shabala,et al.  The Venus Flytrap Dionaea muscipula Counts Prey-Induced Action Potentials to Induce Sodium Uptake , 2016, Current Biology.

[94]  M. Goldman,et al.  Balanced Cortical Microcircuitry for Spatial Working Memory Based on Corrective Feedback Control , 2014, The Journal of Neuroscience.

[95]  J. Holopainen,et al.  Molecular plant volatile communication. , 2012, Advances in experimental medicine and biology.

[96]  Pierre Bonnet,et al.  Plant Responses to High Frequency Electromagnetic Fields , 2016, BioMed research international.

[97]  K. Cunningham,et al.  Calcineurin: Roles of the Ca2+/calmodulindependent protein phosphatase in diverse eukaryotes , 2004 .

[98]  H. Cline Activity-dependent plasticity in the visual systems of frogs and fish , 1991, Trends in Neurosciences.

[99]  E. Fuchs,et al.  Inflammatory Memory Sensitizes Skin Epithelial Stem Cells to Tissue Damage , 2017, Nature.

[100]  Alexander A. Borbély,et al.  Learning by Association in Plants , 2016, Scientific Reports.

[101]  Heribert Hirt,et al.  Multiple roles of MAP kinases in plant signal transduction , 1997 .

[102]  G. Bi,et al.  Synaptic modification by correlated activity: Hebb's postulate revisited. , 2001, Annual review of neuroscience.

[103]  Arun Richard Chandrasekaran,et al.  Addressable configurations of DNA nanostructures for rewritable memory , 2017, Nucleic acids research.

[104]  Kenji Hashimoto,et al.  Calcium Signals: The Lead Currency of Plant Information Processing , 2010, Plant Cell.

[105]  A. Trewavas,et al.  Calcium signalling in Arabidopsis thaliana responding to drought and salinity. , 1997, The Plant journal : for cell and molecular biology.

[106]  Michael Renton,et al.  Tuned in: plant roots use sound to locate water , 2017, Oecologia.

[107]  D. Shohamy,et al.  Feedback Timing Modulates Brain Systems for Learning in Humans , 2011, The Journal of Neuroscience.

[108]  Edi Barkai,et al.  A non-synaptic mechanism of complex learning: Modulation of intrinsic neuronal excitability , 2017, Neurobiology of Learning and Memory.

[109]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[110]  J. Schultz,et al.  Rapid Changes in Tree Leaf Chemistry Induced by Damage: Evidence for Communication Between Plants , 1983, Science.

[111]  Christian Fankhauser,et al.  Sensing the light environment in plants: photoreceptors and early signaling steps , 2015, Current Opinion in Neurobiology.

[112]  Francisco Calvo Garzón,et al.  The quest for cognition in plant neurobiology. , 2007, Plant signaling & behavior.

[113]  Viktor Zárský,et al.  Plant intelligence , 2009, Plant signaling & behavior.

[114]  R. Davenport,et al.  Glutamate receptors in plants. , 2002, Annals of botany.

[115]  Janet Braam,et al.  In touch: plant responses to mechanical stimuli. , 2004, The New phytologist.

[116]  A. Volkov,et al.  Signal transduction in Mimosa pudica: biologically closed electrical circuits. , 2010, Plant, cell & environment.

[117]  Anthony Trewavas,et al.  Intelligence, Cognition, and Language of Green Plants , 2016, Front. Psychol..

[118]  B. Epel,et al.  Plasmodesmata: composition, structure and trafficking , 1994, Plant Molecular Biology.

[119]  G L Shaw,et al.  Model of cortical organization embodying a basis for a theory of information processing and memory recall. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[120]  R. Zweifel,et al.  Ultrasonic acoustic emissions in drought-stressed trees--more than signals from cavitation? , 2008, The New phytologist.

[121]  Juha Pulkkinen,et al.  Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants--a mechanism for associational herbivore resistance? , 2010, The New phytologist.