Neuronal Molecules In Plants

Transcription

1 Neuronal Molecules In Plants Plant Intelligence & more. Communication in Plants: Neuronal Aspects of Plant Life Bonn, 8 November 2006

2 OVERVIEW A) Plant Intelligence B) Action Potentials and Synapses C) Auxin as Plant Neurotransmitter D) Root Apices as Plant Command Centres E) Diffuse Nervous System in Plants? F) Neuronal Molecules in Plants G) Outlook

3 Plant Intelligence Aristoteles (~280 B.C.): Plants have Soul and Feelings Darwin (1880): Plants have Diffuse Brain within Root Apices It is hardly an exaggeration to say that the tip of the radicle thus endowed [with sensitivity] and having the power of directing the movements of the adjoining parts, acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense-organs, and directing the several movements. Page 573 In: The Power of Movement in Plants by Charles Darwin, Assisted by Francis Darwin. John Murray, London, 1880

4 Plant Intelligence 1873 John Burdon-Sanderson: Action Potentials in Leaf Trap of Dionaea Julius von Sachs: Not Possible, Plants do not have Neurons Wie könnten Pflanzen nervenähnlichen Signale weiterleiten, wenn sie keine Nerven haben? Nein, das mußte eine Nebenwirkung eines wichtigeren Informationsträger sein, vielleicht von einem Wasserstrom durch die Falle. Burdon-Sanderson J (1873) Note on electrical phenomena which accompany irritation of the leaf of Dionaea muscipula in the excited and unexcited states. Proc R Soc London 21:

5 Plant Intelligence Bose JC (1926) The Nervous Mechanism of Plants. London, New York: Langmans, Green & Co. Simons P (1992) The Action Plant. Blackwell Publishers, Oxford, UK Roschina VV (2001) Neurotransmitters in Plant Life. Enfield: Science Publisher, New Hampshire, USA Baluska F et al. (2006) Communication in Plants. Neuronal Aspects of Plant Life. Springer Verlag

6 Plant Intelligence Plants are Masters of Adaptation A) Effective and Rapid Sensing of Environmental Signals B) Effective and Rapid Long-Distance Communication C) Effective Information Processing D) Learning and Memory E) Adaptive Responding Trewavas A (2003) Aspects of plant intelligence. Ann Bot 92: 1-20

7 Plant Intelligence Sessile Lifestyle and Phenotypic Plasticity Plant Organs Show Exploratory Behaviour to Achieve Maximal Fitness in Given Environment Trewavas A (2003) Aspects of plant intelligence. Ann Bot 92: 1-20

8 Plant Intelligence Sessile Lifestyle and Phenotypic Plasticity Light and Gravity: Critical Environmental Factors in Shaping Plant Bodies and Positioning of Plant Organs in Time and Space

9 Long-Distance Signal Transmission in Plants A) Translocation of Hormones B) Hydraulic Surge Followed by Variation Potentials C) Action Potentials

10 Action Potentials in Plants Discovered by John Burdon-Sanderson in 1873 The Most Rapid Mean of Long- Distance Communication Which is Based on Excitable Plant Cells Davies E (1987) Action potentials as multifunctional signals in plants: a unifying hypothesis to explain apparently disparate wound responses. Plant Cell Environm 10:

11 Action Potentials in Plants A) Stable Velocity (~1cm/s) B) Propagation Without Decrement C) All-or-None Character of Response D) Excitability Shows Periodicity E) Excitation Induces Morphogenic Movements Zawadzki T et al. (1991) Characteristics of action potentials in Helianthus annuus. Physiol Plant 83:

12 Synapses Term was Coined by Charles Scott Sherrington in 1897 for Neurons Current Broader Definition: Asymmetric Actin-Based Adhesion Domains Specialised for Rapid Cell-to-Cell Communication Dustin ML, Colman DR (2002) Neural and immunological synaptic relations. Science 298:

13 Synapses A) Neuronal Synapses B) Immunological Synapses C) Infectious Synapses D) Plant Synapses

14 Plant Synapses Developmental Auxin-Based Synapses Baluška F et al (2003) Polar transport of auxin: Carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol 13:

15 Plant Synapses in Roots Developmental Auxin-Based Synapses PIN1 Presynaptic Space Vesicle-Based Recycling of Auxin Carriers (PIN1 and AUX1) at Plant Synapses Postsynaptic Space AUX1 Blue: PIN1 (Auxin Efflux Carrier) Red: AUX1 (Auxin Influx Carrier) Green: Actin Black Arrows: Actin-Driven Vesicle Recycling Baluška F et al (2003) Polar transport of auxin: Carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol 13:

16 Plant Synapses in Roots Actin Developmental Auxin-Based Synapses Myosin VIII Actin Myosin VIII Profilin Dynamins ROPs MAPKs Baluška F, Barlow PW, Volkmann D (2000) Actin and myosin VIII in developing root cells. In: Actin: A Dynamic Framework For Multiple Plant Cell Functions, CJ Staiger, F Baluška, D Volkmann, PW Barlow (eds), Kluwer Academic Publishers, Dordrecht, The Netherlands,

17 Auxin as Plant Neurotransmitter A) Vesicular Transport of Auxin Across Plant Synapses B) Auxin Resembles Glutamate in Many Respects C) Extracellular Auxin Induces Electrical Responses Baluška F et al (2003) Polar transport of auxin: Carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol 13:

18 Auxin as Plant Neurotransmitter Extracellular Auxin Induces Electrical Responses in Plant Cells Vorobiev LN, Manusadzianas L (1983) Bioelectrical reactions of Nitellopsis obtusa induced by auxin. Physiol Plant 59: Pickard BG (1984) Voltage transients elicited by sudden step-up of auxin. Plant Cell Environm 7: Goldsworthy A, Mina MG (1991) Electrical patterns of tobacco cells in media containing auxin and 2,4-D. Planta 183:

19 Ward JM et al (1995) Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 7: Electric Excitability of Plant Plasma Membrane Surge of Extracellular Auxin Plasma Membrane Depolarization Increase of Cytoplasmic Calcium Secretion of Neurotransmitter-Like Auxin?

20 Actin Cytoskeleton and Auxin B A Transport Machinery Define Apical-Basal Axis of f Polarity AUX1 ACTIN PIN1 Hypothetical Root Cell AUXIN: - Morphogen-Like - Hormone-Like s - Neurotransmitter-Like Polar Transport of Auxin Along the Apical-Basal Axis of Polarity

21 Plant-Specific Basis of f Multicellularity: Assembly of f Cells into Longitudinal Files B Root Cell File AUX1 PIN1 AUX1 A PIN1 PIN1 AUX1 PIN1 AUX1 AUX1 AUX1 PIN1 AUX1 PIN1 AUX1 Apical- Basal Axis of Polarity Pit- Field PIN1 PIN1 Cross-Walls (PLANT SYNAPSES) Plasmodesmata Baluška et al (2003) BioEssays 25:

22 Maize Root Apex C C Developmental Zones B Elongation Region S IC IC Transition Zone * * A Meristem Apical-Basal Axis of f Polarity Baluška et al (2001) Dev Biol 236:

23 Root Apices as Plant Command Centres Network of Auxin Transporters in the Root Apex Blilou I et al. (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44

24 Root Apex of Arabidopsis: Zones of Plant Brain Elongation Region Transition Zone Meristem Vestibular Organ Root Cap Verbelen J-P, J De Cnodder T, Le J, Vissenberg K, Baluška F (2006) The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic ic zone, transition zone, fast elongation zone and growth terminating zone. Plant Signal Behav, B In press

25 Root Apices as Plant Command Centres? Why not Shoot Apices? Root Apices are Protected from Predatory Activities and from Destructive Impacts of Dramatic Changes in Environment Complex Redistribution of Auxin with Highest Number of Plant Synapses in the Transition Zone and Auxin Maximum in QC/RC Zonation of Root Apices Allowing Synchronization of Cellular Activities and Electrical Responses Exploratory Nature of Root Growth Allows Root Apices to Search for Water, Oxygen, and Nutrients and to Avoid Patches of Soil with Low Water and Oxygen, or Enriched with Heavy Metals

26 Root Apices as Plant Command Centres? Three Sensoric Regions Close Together: A) Root Cap Statocytes (RCS) B) Quiescent Centre (QC) C) Transition Zone (TZ) Auxin Maximum & Redistribution (RCS, QC)

27 Root Apices as Plant Command Centres? Transition Zone Root Apex Transition Zone has the Highest Number of Auxin-Based Synapses Root Apex Transition Zone is Extremely Sensitive Towards External Auxin (Plant Neurotransmitter)

28 Root Apices as Plant Command Centres? Transition Zone A) High Oxygen Consumption B) Aluminium Induces Efflux of Glutamate Dennison KL and Spalding EP (2000) Glutamate-gated calcium fluxes in Arabidopsis. Plant Physiol 124: Sivaguru M et al (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: Evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44:

29 Root Apices as Plant Command Centres? Transition Zone In Root Apex, the Transition Zone is the Largest Sink for Oxygen Resembling Brain Root Apex Transition Zone Shows Rhythmic Oscillations in Oxygen and Potassium Uptake

30 Root Apices as Plant Command Centres? Transition Zone: Synchronous Oscillations of Anatomically Grouped Root Cells Synchrony and Oscillatory Patterning of Anatomically Grouped Neurons Drive Sensorimotor Networks in Brains Engel AK et al (2001) Dynamic predictions: Oscillations and synchrony in top-down processes. Nat Rev Neurosci 2: Harris KD et al. (2003) Organization of cell assemblies in the hippocampus. Nature 424:

31 Root Apices as Plant Command Centres? Oxygen Uptake Into the Transition Zone is Responsive to Gravistimulation of Root Apices Oxygen Uptake Into the Transition Zone is Responsive to Wounding and Mechanical Stimulation of Shoot Apices Each of These Shoot Stresses Elicited Unique Signature in the Oxygen Uptake Response in the Transition Zone Oxygen Uptake is Sensitive to Auxin Transport Inhibitors (TIBA, NPA) and Inhibitor of Secretion Brefeldin A (BFA) Mancuso S et al. Unpublished Data

32 Root Apices as Plant Command Centres? The Speed of these Rapid Responses (4-5 Seconds in About 10 cm Long Maize Seedlings) Suggests that Action Potentials Mediate this Telecommunication. In Support of this Attractive Notion, Action Potential was Recorded 2-3 Seconds Before the Oxygen Uptake Responses. These Data Corresponds to Measurements on Single Activated Neurons (Thompson et al. 2003). Thompson D et al (2003) Science 299:

33 Diffuse Nervous System in Plants? Lower Animals, Like Echinoderms and Hemichordates, do not have Central Nervous System (CNS) but have Diffuse Nervous System (DNS) Recent Milestone Paper Revealed that CNS Evolved From DNS and That Diffuses Nerve Net of DNS is Embedded within Epithel and Encircles the Whole Body of these Lower Animals (Lowe et al. 2003). Lowe CJ et al (2003) Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113:

34 Diffuse Nervous System in Plants? In Brains, Phenotypic Plasticity of Neurons Underpins Learning and Memory Processes. In Plants, Phenotypic Plasticity of the Whole Plant Body Supports the Diffuse Nervous System of Plants. Cells within the Individual Plant Cell Files are Interconnected via Actin-Based Plant Synapses (End-Poles of Elongating Cells) which: Transport Polarly Plant Neurotransmitter Auxin

35 Nervous Molecules in Plants Synaptic Proteins: Synaptotagmins, SNAP25, Glutamate Receptors, Synaptic Tetraspannin Proteins, Copines,.. Classical Neurotransmitters: Glutamate, GABA (γ-aminobutyric Acid), Dopamine, Acetylcholine, ATP,

36 Nervous Molecules in Plants Ligands/Antagonists of Glutamate Receptors: Kainate, BMAA, Neurologically Active Substances: Tein, Caffein, Nicotin, Cocaine, Cannabis, Serotonin, Histamine, Plant Homologues of Vesicular Neurotransmitter Transporters: PIN1, AUX1,

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42 Plant Synapses Blue Light Photoreceptor PHOT1 Arabidopsis thaliana GFP-PHOT1 PHOT1 Green, FM4-64 Red Yinglan Wan

43 Plant Synapses Myosin VIII Wall-Associated Kinase 1 (WAK1) Arabidopsis thaliana Thorsten Lasse

44 Auxin Immunolocalization Auxin Localizes to Root Synapses and Endosomal BFA-induced Compartments Control BFA Zea mays Markus Schlicht

45 Zea mays Markus Schlicht / Alina Schick Plant Synapses Meristem PIN1

46 Plant Synapses Transition Zone Stele (Vascular Cylinder Cortex PIN1 Zea mays PIN1 Markus Schlicht / Alina Schick

47 Synaptotagmins at Plant Synapses Synaptotagmins are Neuronal Proteins Mediating Calcium Regulated Exocytosis and Endocytosis at Neural Synapses Arabidopsis Genome Encodes Six Synaptotagmin Genes Arabidopsis Synaptotagmins Localize to Plant Synapses in Root Cells of the Transition Zone Plant Synapses as Signaling Domains: PHOT1, WAK1, BRI1, AtSERKs, MAPKs, Rops

48 Plant Synapses Synaptotagmins at Root Synapses Arabidopsis thaliana Boris Voigt Molly Craxton Bazbek Davletov MRC Neurobiology Cambridge, UK

49 Plant Synapses Synaptotagmins at Root Synapses

50 Plant Synapses Synaptotagmins at Stomata Synapses Boris Voigt Stable Expression of AtSytA in Arabidopsis seedlings

51 Synaptic Cell-Cell Communication in Plants 22 November