Auxin Modulated Initiation of Lateral Roots Is Linked to Pericycle Cell Length in Maize

Abstract

Auxin is essential for the regulation of root system architecture by controlling primary root elongation and lateral root (LR) formation. Exogenous auxin has been reported to inhibit primary root elongation and promote the formation of LRs. In this study, LR formation in the Zea mays primary root was quantitatively evaluated after exogenous auxin treatment by comparing the effects of auxin on two selected zones elongated either before or after auxin application. We determined two main variables in both zones: the LR density per unit of root length (LRD), and the mean phloem pericycle cell length. The total number of phloem pericycle cells (PPCs) per unit of root length was then calculated. Considering that each LR primordium is initiated from four founder cells (FCs), the percentage of PPCs (%PPC) that behave as FCs in a specific root zone was estimated by dividing the number of pericycle cells by four times the LRD. This index was utilized to describe LR initiation. Root zones elongated in the presence of a synthetic auxin (1-naphthalene acetic acid, NAA) at low concentrations (0.01 μM) showed reduced cell length and increased LRD. However, a high concentration of NAA (0.1 μM) strongly reduced both cell length and LRD. In contrast, both low and high levels of NAA stimulated LRD in zones elongated before auxin application. Analysis of the percentage of FCs in the phloem pericycle in zones elongated in the presence or absence of NAA showed that low concentrations of NAA increased the %PFC, indicating that LR initiation is promoted at new sites; however, high concentrations of NAA elicited a considerable reduction in this variable in zones developed in the presence of auxin. As these zones are composed of short pericycle cells, we propose that short pericycle cells are incapable to participate in LR primordium initiation and that auxin modulated initiation of LRs is linked to pericycle cell length.

Keywords: Zea mays; auxin action; cell growth; lateral root development; maize; pericycle; root elongation.

FIGURE 1

Formation of two 2-cm long consecutive zones in the maize primary root after NAA application. At time 0, treatment was performed by applying NAA to the growth medium (1). Zone A (filled) is elongated before auxin application, hence cell elongation occurred without auxin influence. In contrast, zone B (unfilled) elongated in the presence of auxin. Subsequently, the root grows and lateral roots develop in both zones under the influence of exogenous auxin. Note that after 48 h, root elongation was greater in control (2) than in auxin-treated roots (3).

FIGURE 2

Effect of 0.01 μM NAA treatment on lateral root density (LRD) in the maize primary root. LRD was measured in 2-cm-long root segments from the base to the root tip. Auxin was applied when the roots were 8 cm long and LR formation was followed during a subsequent 48 h period. Note the inhibitory effect of NAA on root elongation and the stimulating effect on LRD in the youngest root zones analyzed. Values represent mean ± SD (n = 10).

FIGURE 3

Effects of several NAA concentrations on lateral root (LR) formation and primary root elongation within 48 h after NAA application. Number of LRs plus LR primordia (A), primary root elongation (B), and average LRD (C) in the formed segments of primary maize roots. Values are mean ± SD (n = 10). Different letters indicate significant differences at P < 0.05 (ANOVA and Tukey’s test).

FIGURE 4

The junction between zones A and B in 0.1 μM NAA-treated maize roots. Micrograph of a maize root fragment at the junction between zones A and B (arrow). Note that zone A zone is thinner and shows a high LRD with numerous emerged lateral roots (LRs). In contrast, zone B is thicker, with relatively few un-emerged LRs. Scale bar = 1 mm.