Root apex transition zone as oscillatory zone

Abstract

Root apex of higher plants shows very high sensitivity to environmental stimuli. The root cap acts as the most prominent plant sensory organ; sensing diverse physical parameters such as gravity, light, humidity, oxygen, and critical inorganic nutrients. However, the motoric responses to these stimuli are accomplished in the elongation region. This spatial discrepancy was solved when we have discovered and characterized the transition zone which is interpolated between the apical meristem and the subapical elongation zone. Cells of this zone are very active in the cytoskeletal rearrangements, endocytosis and endocytic vesicle recycling, as well as in electric activities. Here we discuss the oscillatory nature of the transition zone which, together with several other features of this zone, suggest that it acts as some kind of command center. In accordance with the early proposal of Charles and Francis Darwin, cells of this root zone receive sensory information from the root cap and instruct the motoric responses of cells in the elongation zone.

Keywords: auxin; neurotransmitter agents; plant communication; plant cytoskeleton; plant electrophysiology; plant morphogenesis; plant polarity; plant roots; plant sensory biology.

FIGURE 1

Transition zone as oscillatory zone. Oscillations of the plasma membrane electrical potentials generate, via multiple feedback loops with membrane associated cytoskeleton, self-sustaining and self-regulating cellular oscillator (Shabala et al., 1997, 2006; Mancuso and Boselli, 2002; Shabala, 2003; Mancuso et al., 2005, 2007; McLamore et al., 2010a, b; Mugnai et al., 2012). Oscillatory patterns of ion and auxin fluxes at the plasma membrane feed into the oscillations of gene expression in the nucleus (Moreno-Risueno et al., 2010, 2012; Traas and Vernoux, 2010; Moreno-Risueno and Benfey, 2011). M, meristem; TZ, transition zone; EZ, elongation zone.

FIGURE 2

Schematic view of the transition zone cell and its auxin-secreting synapse. (A) Cells in the transition zone maintain their nuclei in the central position. Instead of fine F-actin networks typical for meristematic cells, these cells develop prominent bundles of F-actin which enclose the nucleus in a cage-like structures. Inhibition of endocytic vesicle recycling with brefeldin A results in a disintegration of this F-actin cage and nuclei are shifted out of their central position (Baluška and Hlavacka, 2005). At the plasma membrane, F-actin bundles are anchored at F-actin rich end-poles which are active in endocytosis/endocytic vesicle reycling. Anchoring of F-actin bundles at the plasma membrane and support of dense F-actin meshorks at these domains is accomplished via myosin VIII, group Ie formins, and NET1A actin-binding protein (Baluška et al., 1997, 2000c, 2002, 2009a; Deeks et al., 2005, 2012; Baluška, 2012a). (B) Abundant myosin VIII, dense meshworks of F-actin, and very active endocytosis of cell wall pectins crosslinked with boron and calcium allow tight synaptic cell–cell adhesion. At these adhesive and polar cell domains, cells secrete auxin out cells via the endocytic vesicle recycling of pectins and numerous plasma membrane proteins including putative auxin transporters of the PIN family (Baluška et al., 2002, 2008; Mancuso et al., 2005, 2007). Auxin is peceived at the adjacent cells via its plasma membrane/cell periphery receptor ABP1. Glutamate is proposed also to be secreted out of plant cells and glutamate receptor-like protein GLR3.3 is enriched at these synaptic domains (see Figure 1C in Vincill et al., 2013).

FIGURE 3

Schematic views of cellular architecture in meristem, transition zone and elongation region. Cells in the meristem are characterized with centrally positioned nuclei suspended in networks of F-actin and radial arrays of perinuclear microtubules (Baluška et al., 1992, 1997, 2000c; Voigt et al., 2005b). In the transition zone, nuclei still keep their central position, but fine F-actin networks are replaced by bundles of F-actin organized via the nuclear surface and the end-poles enriched with myosin VIII (Baluška et al., 1997, 2000c; Reichelt et al., 1999). In the elongation region, cells start to elongate very rapidly and develop their central vacuole which is pushing their nuclei toward the side walls. F-actin bundles obtain longitudinal and wrinkled/loosened appearances (Baluška et al., 1997, 2000c; Voigt et al., 2005b).

FIGURE 4

Schematic views of cellular root apex zones and their electric fields. Sensory root cap is enclosing the meristem with dividing cells. These two most apical zones are characterized by the outward electric current (Collings et al., 1992; Baluška and Mancuso, 2013a). Adjacent transition zone is characterized with two inversions of the electric current pattern at the root apex. The apical border of the transition zone accomplishes the outward–inward switch whereas the basal border the inward–outward switch (Collings et al., 1992; Baluška and Mancuso, 2013a). The elongation region is characterized again by the outward electric current. High root synaptic activities at the transition zone are linked with the prominent inward electric currents.

FIGURE 5

Schematic views of two loops of the polar auxin transport streams at the root apex. In the central stelar tissue, polar auxin transport stream is polarized toward the root cap. Here it is redistributed laterally in a fountain-like manner toward the root periphery at which the stream gets opposite (shootward) polarity and continues up to the basal border of the transition zoner, where it is looping back via an inversed fountain-like manner back to the central stelar tissues. This complex pattern of polar cell–cell transport of auxin is tightly linked with sensory events at the root cap and instruct the motoric events at the apical portion of the elongation region (Baluška et al., 2009a, b, 2010a; Baluška and Mancuso, 2013a).

FIGURE 6

BFA inhibits oxygen influx peak into the transition zone. Effect of different concentrations of BFA on the profiles of the oxygen influx for the upper side in maize roots growing vertically for 5 min after gravistimulation (elicited by rotating the chamber 90^° until the root was horizontal. Values are means, n = 15. Oxygen fluxes were measured with a vibrating oxygen-selective microelectrode following the method described in Mancuso et al. (2000).