Neurobiology: Trends in Plant Science.

suchandra · May 4, 2007

Although modern Neurobiology doesnt consider that within plants there's is a soul they say that they are able to scientifically prove that plants have intelligence to make decisions or to successfully persist in a certain position. A tree on top of a mountain uses a different strategy to grow than the same tree planted in a valley.

sciencedirect.com

The past three years have witnessed the birth and propagation of a provocative idea in the plant sciences.Its proponents have suggested that higher plants have nerves, synapses, the equivalent of a brain localized somewhere in the roots, and an intelligence. The idea has attracted a number of adherents, to the extent that meetings have now been held in different host countries to address the topic, and an international society devoted to ‘plant neurobiology’ has been founded. We are concerned with the rationale behind this concept. We maintain that plant neurobiology does not add to our understanding of plant physiology, plant cell biology or signaling. We begin by stating simply that there is no evidence for structures such as neurons, synapses or a brain in plants. The fact that the term ‘neuron’ is derived from a Greek word describing a ‘vegetable fiber’ is not a compelling argument to reclaim this term for plant biology. Let usconsider the erroneous arguments that have been put forward to support the concept of plant ‘neurons’. By this logic, cells that contribute to auxin transport are equated to chains of neurons, and it is argued that auxin transport occurs via a concerted vesicle-based trafficking mechanism of ‘neurotransmitter-like cell–cell transport’ [1,2]. Thereare two immediate difficulties with this reasoning.(i) Neurotransmitters are not transported from cell to cell over long distances. (ii) The evidence that auxin is sequestered within exocytic vesicles is weak [3]. This notion is difficult to reconcile with the acknowledged distribution and function of the PIN and AUX families of auxin transporters, which locate to different polar domains of the plasma membrane [4] and cycle to and from endosomal compartments to the plasma membrane under the controlof auxin [5]. Together with the P-glycoprotein subfamily of ABC auxin transport proteins [6], which appear to function coordinately with PIN efflux carrier proteins [7], the setransport activities are sufficient to account for the known rates of polar auxin transport, and do not sit comfortably with the idea of vesicle-mediated traffic of auxin, even oversub-cellular distances. Another fundamental stumbling block regarding theconcept of plant neurobiology is the common occurrence of plasmodesmata in plants. Their existence poses a problem for signaling from an electro physiological point of view – extensive electrical coupling would preclude the need for any cell-to-cell transport of a ‘neurotransmitter-like’ compound – leading Eric Brenner et al. [2] to argue that ‘these cytoplasmic connections have a poorly described role in electrical coupling between adjacent polarized plantcells’. In fact, huge numbers of plasmodesmata occur between cells that contribute to polar auxin transport, but their existence has been neglected within the plant hormone research field. Given the existence of plasmodes-mata, there is no a priori reason why plant hormones should not be transported symplastically through the cytosol. Indeed, the presence of influx and efflux transporters for auxin at the plasma membrane suggests that auxinis present in the cytosol. So either auxin is effectively excluded at plasmodesmata, or it does not enter the cytosol until it reaches cells of the extension zone where it is takenup and then released to exert its effects. Clearly, there are still many unknowns surrounding auxin transport, and therole (if any) of plasmodesmata in this process remains as enigmatic as it was almost 15 years ago [8]. It could be argued that auxin is taken up in vesicles via endocytosisand moves by vesicular traffic to the opposing plasma membrane where it is released by exocytosis, and that this process is continually repeated along the axis of transport. However, this model should not be confused with events in nerves and at the synapse. So, are we better informed scientifically about these unknowns, or better guided towards their resolution, by the plant neurobiology concept? Plant cells do share fea-tures in common with all biological cells, including neurons. To name just a few: plant cells show action potentials, their membranes harbor voltage-gated ionchannels, and there is evidence of neuro transmitter-like substances. Equally, in a broader sense, signal transduction and transmission over distance is a property of plants and animals. Although at the molecular level the same general principles apply and some important parallels can be drawn between the two major organismal groups, this does not imply a priori that comparable structures for signal propagation exist at the cellular, tissue and organ levels. A careful analysis of our current knowledge of plant and animal physiology, cell biology and signaling provides no evidence of such structures. New concepts and fields of research develop from the synthesis of creative thinking and cautious scientific analysis. True success is measured by the ability to foster new experimental approaches that are founded on the solid grounding of previous studies.

What long-term scientific benefits will the plant science research community gain from the concept of ‘plant neurobiology’? We suggest these will be limited until plant neuro biology is no longer founded on superficial analogies and questionable extra-polations. We recognize the importance of a vigorous and healthy dialog and accept that, as a catch-phrase, ‘plantneurobiology’ has served a purpose as an initial forum for discussions on the mechanisms involved in plant signaling. We now urge the proponents of plant neurobiology to reevaluate critically the concept and to develop an intellectually rigorous foundation for it.

References

1 Baluška, F. et al. (2005) Plant synapses: actin-based domains for cell-to-cell communication. Trends Plant Sci. 10, 106–1112 Brenner, E.D. et al. (2006) Plant neurobiology: an integrated view ofplant signaling. Trends Plant Sci. 11, 413–4193 Schlicht, M. et al. (2006) Auxin immunolocalization implicates avesicular neurotransmitter-like mode of polar auxin transport in rootapices. Plant Signal Behav. 1, 122–1334 Kleine-Vehn, J. et al. (2006) Subcellular trafficking of the Arabidopsisauxin influx carrier AUX1 uses a novel pathway distinct from PIN1.Plant Cell 18, 3171–31815 Paciorek, T. et al. (2005) Auxin inhibits endocytosis and promotes itsown efflux from cells. Nature 435, 1251–12566 Geisler, M. and Murphy, A.S. (2005) The ABC of auxin transport: therole of P-glycoproteins in plant development. FEBS Lett. 580, 1094–11027 Blakeslee, J.J. et al. (2007) Interactions among PIN-FORMED andP-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19,131–1478 Oparka, K.J. (1993) Signalling via plasmodesmata – the neglectedpathway. Semin. Cell Biol. 4, 131–138136UpdateTRENDS in Plant Science Vol.12 No.4www.sciencedirect.com

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