The production and release of living root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants

Abstract

Background and aims: The root apical meristems (RAM) of flowering plant roots are organized into recognizable pattern types. At present, there are no known ecological or physiological benefits to having one RAM organization type over another. Although there are phylogenetic distribution patterns in plant groups, the possible evolutionary advantages of different RAM organization patterns are not understood. Root caps of many flowering plant roots are known to release living border cells into the rhizosphere, where the cells are believed to have the capacity to alter conditions in the soil and to interact with soil micro-organisms. Consequently, high rates of border cell production may have the potential to benefit plant growth and development greatly, and to provide a selective advantage in certain soil environments. This study reports the use of several approaches to elucidate the anatomical and developmental relationships between RAM organization and border cell production.

Methods: RAM types from many species were compared with numbers of border cells released in those species. In addition, other species were grown, fixed and sectioned to verify their organization type and capacity to produce border cells. Root tips were examined microscopically to characterize their pattern and some were stained to determine the viability of root cap cells.

Key results: The first report of a correlation between RAM organization type and the production and release of border cells is provided: species exhibiting open RAM organization produce significantly more border cells than species exhibiting closed apical organization. Roots with closed apical organization release peripheral root cap cells in sheets or large groups of dead cells, whereas root caps with open organization release individual living border cells.

Conclusions: This study, the first to document a relationship between RAM organization, root cap behaviour and a possible ecological benefit to the plant, may yield a framework to examine the evolutionary causes for the diversification of RAM organization types across taxa.

Fig. 1.

Graph illustrating that roots with closed organization (triangles) have few to no border cells, and those with open organization [intermediate-open (open squares) and basic-open (closed squares)] tend to release border cells. Border cell number data from Hawes et al. (2003) and root apical meristem organization data from Groot et al. (2004).

Fig. 2.

(A) Scanning electron micrograph of the tip of a Brassica napus root showing external view of the root cap. (B) Longitudinal section of a closed root apical meristem showing initial tiers and root cap layers peeling off. (C) Transverse view. Individual border cells do not occur. Scale bars = 90 μm.

Fig. 3.

(A) Scanning electron micrograph of Helianthus annuus root tip. (B) An example of intermediate-open root apical meristem organization in longitudinal view. (C) Transverse view showing border cells. Scale bars = 60 μm (A), 90 μm (B and C).

Fig. 4.

(A) Scanning electron micrograph of Pisum sativum root tip. (B) Longitudinal view showing basic-open root apical meristem organization. (C) Transverse view showing released border cells. Scale bars = 105 μm.

Fig. 5.

(A) Whole mount of Brassica napus root tip. (B) Same root tip stained with fluoroscein diacetate shows no staining on the root cap periphery, indicating no living cells. Scale bar = 70 μm.

Fig. 6.

(A) Whole mount of Helianthus annuus root tip. (B) Same root tip showing positive fluoroscein diacetate staining of released border cells. Scale bar = 46 μm.

Fig. 7.

(A) Whole mount of Pisum sativum root tip. (B) Same root tip showing positive fluoroscein diacetate staining of border cells. Scale bar = 57 μm.