Root apex transition zone as oscillatory zone

As already mentioned, GLRs are enriched in phloem, especially at the sieve plates (Vincill et al., 2013), close to the root apex where phloem is unloaded (Baluška et al., 2001c). Importantly in this respect, both the phloem transport and the phloem unloading are controlled electrically via action potentials (Fromm, 1991; Fromm and Bauer, 1994; Fromm and Lautner, 2006).

In contrast to the shoot apex, the plant root apex is highly regularly organized with clearly defined zones (Figures 2 and 3) and regular cell files (Ishikawa and Evans, 1995; Baluška et al., 1996b, 2006b, 2010a; Verbelen et al., 2006; Ivanov and Dubrovsky, 2013). It is very interesting that this anatomical zonation is associated with clear patterns of electric activities when root cap and elongation region show outward electric currents (Figure 4), whereas meristem and especially the transition zone generates prominent inward electric currents (Collings et al., 1992; Figure 4). Importantly, these electric activities not only peak but also oscillate in the transition zone (Masi et al., 2009), where also auxin fluxes oscillate (McLamore et al., 2010a, b), and the root growth rates are tightly linked with the electric currents oscillations (Souda et al., 1990; Hecks et al., 1992). Anoxia or ether exposures block the currents oscillations (Yoshida et al., 1988) and root growth (Hecks et al., 1992), whereas recovery of the root growth is linked with the re-appearance of electric currents oscillations (Hecks et al., 1992). Furthermore, oscillatory patterns of ion transport activities and electric currents at the transition zone of barley root apices are closely linked with the rhythmic patterns of nutrient acquisition (Shabala and Knowles, 2002). In future studies, it will be important to find out further details of this oscillatory strategy for root nutrient acquisition. On the other hand, these root apex-specific electric currents can feed back not only into growth processes but also into morphogenesis of root apex as cell division patterns in maize root apices are sensitive to the extracellular electric fields (Wawrecki and Zagórska-Marek, 2007). In plants, these studies are very few and our knowledge extremely limited.

But in animals, it is getting obvious that the emerging bioelectric code is at least as important for the development, embryogenesis and regeneration as the genetic code (Tseng and Levin, 2013). Any living cells, and even their organelles, generate their own electric fields which feedback into the biochemical and molecular processes underlying the cell/tissue polarities (McCaig et al., 2009; Yao et al., 2009; Zhao et al., 2012; Tseng and Levin, 2013). Endocytosis emerges to be sensitive to electric fields. Similarly as in neurons, endosomes of plant cells also process the sensory information for motoric outcomes (behavior) of their organs such as roots (Baluška and Volkmann, 2011; Baluška and Wan, 2012; Wan et al., 2012).

Electric fields generated by the oscillatory transition zone resemble encephalograms scored around brains of animals and humans. These prominent electric fields represent summation of synchronous electric activities of transition zone cells, and suggest two important features of this unique root apex zone. Firstly, the transition zone cells have the highest electric activities from all cells of the whole root (Masi et al., 2009) and; secondly, this activity is highly synchronous (Figure 1). Only this synchronicity allows vibrating probes to detect prominent electric currents which form the characteristic pattern of the smaller outward current peak at the meristematic zone and the prominent inward current peak at the transition zone (Baluška and Mancuso, 2013a). It is still mystery why the polarity of electric current suddenly switches from outward to inward at the meristem–transition zone border (Figure 4). Interestingly, the inward current switches again, back to the outward current at the transition zone–elongation region border (Collings et al., 1992; Baluška and Mancuso, 2013a). This pattern of electric field was scored in roots of all species tested so far, suggesting that there is something special about the inward current of the transition zone (Baluška and Mancuso, 2013a). As it correlates with high activities of root synapses, it might be possible that sensory stimuli/experiences will modify patterns of root electric fields. In support of this attractive possibility, root apex electric fields change during gravistimulation of maize roots (Collings et al., 1992). In addition, the PAT (Figure 5) appears to act as both the sensor and instructor for the adaptive root behavior (Baluška et al., 2009a, b, 2010a, b). The transition zone electric field is affected by inhibitors of PAT (Collings et al., 1992).

In future, it will be important to analyze the possible connections between the synaptic activities and the patterns of the electric fields around the oscillatory transition zone (Figures 1 and 4). Particularly, how do the sensory inputs modify these electric field patterns, and if modified electric field patterns are related to the motoric output of driving the root behavior. Sensory perceptions and active behaviors are linked to neurons and neuronal systems in both lower and higher animals. Currently, the mainstream of plant sciences considers plants for passive automata-like organisms, lacking any sensory-motoric circuits. But this position, which is based on ancient Aristotelian worldviews, depriving plants of cognition-relevant sensitivities and activities are not tenable anymore (Brenner et al., 2006, 2007;Trewavas, 2007, Trewavas, 2009; Barlow, 2008; Baluška, 2009; Calvo and Keijzer, 2010; Karpiński, 2010; and Szechyńska-Hebda, 2010;; Trewavas and Baluška, 2011; Marder, 2012, 2013; Debono, 2013). Especially root behavior shows cognitive features which are not possible to explain with currently dominated views of passive, automata-like organisms (Baluška et al., 2010b; Barlow, 2010a, b; Gagliano et al., 2012).

In humans and animal brains, neuronal oscillations are important for processing of sensory information (Schroeder and Lakatos, 2008; Uhlhaas et al., 2009, 2010; Hipp et al., 2011; Arnal and Giraud, 2012). Synchrony and oscillatory patterning of anatomically grouped neurons drive sensorimotor networks in animals. Similarly in the root apex transition zone, all cells show synchronous oscillations (Figure 1) which are related to root behavior based on plant-specific sensorimotor networks. In future, it will be important to understand possible links between the oscillations at the plasma membrane and gene expression oscillations, as well as the relevance of these oscillations for the brain-like command center status of the transition zone and the whole root apex (Darwin, 1880; Barlow, 2006; Baluška et al., 2009b). It is emerging that besides the plant-specific molecules such as auxin, also many of the classical neuronal molecules including glutamate, GABA, serotonin, melatonin, acetylcholine, will be relevant in this respect.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.