Recent surprising similarities between plant cells and neurons

Abstract

Plant cells and neurons share several similarities, including non-centrosomal microtubules, motile post-Golgi organelles, separated both spatially/structurally and functionally from the Golgi apparatus and involved in vesicular endocytic recycling, as well as cell-cell adhesion domains based on the actin/myosin cytoskeleton which serve for cell-cell communication. Tip-growing plant cells such as root hairs and pollen tubes also resemble neurons extending their axons. Recently, surprising discoveries have been made with respect to the molecular basis of neurodegenerative disorders known as Hereditary Spastic Paraplegias and tip-growth of root hairs. All these advances are briefly discussed in the context of other similarities between plant cells and neurons.

Tip-Growth of Plant Cells and Neurons: From Polarized Secretion to Action Potentials

There are very prominent similarities between tip-growing plant cells and the extending axons of neurons.1,2 However, recent advances reveal that these visible similarities stretch beyond the tip-growing plant cells and include plant tissue cells generating action potentials3 and accomplishing vesicle trafficking and recycling, typically at actin/myosin enriched cell-cell adhesion domains resembling neuronal synapses.4–7 Moreover, plant cells and neurons are similar from the cellular perspective, when most of their microtubules and Golgi apparatus organelles are not associated with the perinuclear centrosomes.8 In plant cells, Golgi stacks and Trans-Golgi Networks (TGNs) are motile organelles extending through the whole plant cells.9 Similarly in neurons centrosome-independent cortical microtubules are abundant in axons. They transport, among other cargo, so-called Golgi Outposts—which correspond to the TGNs of plant cells9—toward neuronal synapses.10–12 In both plant cells and neurons, TGNs act as independent organelles separated both spatially/structurally and functionally from the Golgi apparatus.9–13 Intriguingly, similarly as in neurons, also the TGN of plant cells is the inherent part of the endosomal/vesicular recycling pathways,9,13–15 supporting the dynamic and communicative nature of plant synapses. 4,5,15,16 Plant action potentials (electric spikes) run in an axial direction, along the longitudinal axis of any plant organ,17–19 and the highest spike activity was scored in the transition zone of the root apex in maize.20

Hereditary Spastic Paraplegias (HSP): Root Hairs versus Neurons

Hereditary spastic paraplegia (HSP) represents a heterogeneous group of genetic neurodegenerative disorders affecting the longest neurons of the human body, extending from the brain along the spinal cord /down to the legs.21 In the HSP disorders, axons of these long neurons degenerate causing problems in controlling leg muscles. One of the major genes in which mutation results in the HSP is Atlastin.22 Recent study has reported that Atlastin is homologous to the RHD3 protein of Arabidopsis.23 RHD3 protein is essential for proper growth and development of root hairs in Arabidopsis.24,25 Moreover, RHD3 is also important for the proper arrangement of root cell files which underlies the direction of root growth.26 In order to maintain their ordered cell files, root apex cross-walls (plant root synapses) perform active vesicle recycling.4,5,7 Both Arabidopsis RHD3 and Drosophila Atlastin are important for shaping tubular ER networks.23,27 RHD3 is also known to be required for the proper arrangement of the actin cytoskeleton and cell wall maintenance via vesicle trafficking.28 Moreover, similarly as Atlastin in neurons,31 RHD3 is important for the GA morphogenesis in plant cells too.29 Importantly, both RHD3 and Atlastin are implicated in membrane tubulation and vesiculation whereas rhd3 mutant line emerges to be less active in endocytic internalization of FM4-64 endocytic tracer.29 Drosophila Atlastin regulates the stability of muscle microtubules and is required for both the axonal maintenance and synapse development.30,31,32 All this suggest that Arabidopsis emerges as an attractive and useful model object for investigations of mechanisms underlying HSP disorders in humans.

Neurobiological Roles of Glutamate and Glutamate Receptors in Plants

Glutamate is one of the best understood and the most widespread excitatory neurotransmitter which is perceived via glutamate receptors at brain synapses in animals and humans. These neuronal receptors have, in fact, deep evolutionary origin in prokaryotic bacteria33,34 and are present also in plants.35,36 Importantly, the plant glutamate receptors have all the features of neuronal ones,37 and glutamate induces plant action potentials.18,19 All this strongly suggest that glutamate serves in neurotransmitter-like cell-cell communication in plants too. Interestingly in this respect, especially the root apices are target of the neuronal-like activity of glutamate in plants, with effects on cell development, root growth, morphogenesis, and behavior.38–40 The transition zone cells, localized between the apical meristem and basal cell elongation zone,41,42 respond to glutamate with rapid depolarization of the plasma membrane and this response is blocked by a specific antagonist of ionotropic glutamate receptors, 2-amino-5-phosphonopentanoate.43 Cells of the transition zone, also known as the distal elongation zone or the basal meristem, are crucial for root primordia priming,41,44 and exogenous glutamate is known to decrease primary root growth and increase lateral root proliferation.38,39

Beta-N-methylamino-L-alanine (BMAA) is a neurotoxic amino acid, derived from cycads, which is well-known to act as agonists and antagonists of mammalian glutamate receptors. BMAA inhibits root growth, cotyledon opening, and it stimulates elongation of light-grown hypocotyls in Arabidopsis.45 BMAA affects growth of Arabidopsis organs at very low concentrations, and these BMAA-induced effects are reversed by the addition of glutamate.45,46 This is consistent with a scenario wherein BMAA acts to block plant-specific glutamate receptors.

Neurotoxic Aluminium Targets Active Plant Synapses in the Root Apex Transition Zone

Similarly to glutamate, aluminium also induces very rapid plasma membrane depolarization specifically in cells of the root apex transition zone.43,47 Moreover, glutamate and aluminium both induce rapid and strong calcium spikes with unique signatures in cells of the transition zone.48 These root cells represent the primary target for the aluminium toxicity in plants, whereas aluminium is not toxic to root cells which have already entered the rapid elongation region.49–52 Similarly, although aluminium is not so toxic in most plant cells, neuronal-like tip-growing root hairs and pollen tubes1,2 are sensitive to aluminium53,54 similarly as are the transition zone cells. In these latter cells, aluminium is specifically internalized47,55 via endocytosis.47 Internalized endocytic aluminium interferes with vesicle trafficking/recycling and endocytosis,47,56 inhibiting the PIN2-driven basipetal auxin transport in the transition zone of root apices.51,56 Aluminium targets specifically the auxinsecreting plant synapses51,56,57 and affects the polar auxin-transport-based root cell patterning.52 Moreover, aluminium affects also nitric oxide (NO) production which is highest in cells of the the distal portion of the transition zone.47 Importantly, the rapidly elongating root cells are not sensitive towards aluminium43,49,50 and neither is there internalization of aluminium into rapidly elongating root cells.47,55 In support of the endocytosis of aluminium being the primary process linked to the aluminium toxicity in root cells, endocytosis of aluminium and its toxicity is lowered in the Arabidopsis mutant over-expressing the DnaJ domain protein auxillin which regulates the clathrin-based endocytosis.58

In animals and humans, neuronal cells are extremely sensitive towards aluminium which is internalized via endocytosis specifically in these cells.59–61 Aluminium was found to be enriched in lysosomes, similarly like Alzheimer’s amyloid β-peptide plaque depositions.59–61 These are also internalized from cell surface and aluminium was reported to inhibit their degradation.61

In conclusion, in both transition zone root cells and neurons, endocytosis of aluminium emerges as relevant to its high biotoxicity. In plants, the aluminium toxicity is the most important limiting factor for crop production in acid soil environments worldwide. Further studies on these cells might give us crucial clues not only for plant biology and agriculture but also for our still limited understanding of the Alzheimer disease. In line with the original proposal of Charles and Francis Darwin,62 root apices of plants represent neuronal/anterior pole of plant bodies.63