Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medicinal plant Merwilla plumbea

Abstract

Background and aims: Merwilla plumbea is an important African medicinal plant. As the plants grow in soils contaminated with metals from mining activities, the danger of human intoxication exists. An experiment with plants exposed to cadmium (Cd) was performed to investigate the response of M. plumbea to this heavy metal, its uptake and translocation to plant organs and reaction of root tissues.

Methods: Plants grown from seeds were cultivated in controlled conditions. Hydroponic cultivation is not suitable for this species as roots do not tolerate aquatic conditions, and additional stress by Cd treatment results in total root growth inhibition and death. After cultivation in perlite the plants exposed to 1 and 5 mg Cd L(-1) in half-strength Hoagland's solution were compared with control plants. Growth parameters were evaluated, Cd content was determined by inductively coupled plasma mass spectroscopy (ICP-MS) and root structure was investigated using various staining procedures, including the fluorescent stain Fluorol yellow 088 to detect suberin deposition in cell walls.

Key results: The plants exposed to Cd were significantly reduced in growth. Most of the Cd taken up by plants after 4 weeks cultivation was retained in roots, and only a small amount was translocated to bulbs and leaves. In reaction to higher Cd concentrations, roots developed a hypodermal periderm close to the root tip. Cells produced by cork cambium impregnate their cell walls by suberin.

Conclusions: It is suggested that the hypodermal periderm is developed in young root parts in reaction to Cd toxicity to protect the root from radial uptake of Cd ions. Secondary meristems are usually not present in monocotyledonous species. Another interpretation explaining formation of protective suberized layers as a result of periclinal divisions of the hypodermis is discussed. This process may represent an as yet unknown defence reaction of roots when exposed to elemental stress.

Fig. 1.

Effect of cadmium on 17-week-old Merwilla plumbea plants grown for 4 weeks in (A) hydroponics and (B) perlite. Three different treatments were used: control (C); 1 mg Cd L⁻¹ (Cd1); and 5 mg Cd L⁻¹ (Cd5). Scale bars = 1 cm.

Fig. 2.

Effect of cadmium on fresh weight of 17-week-old Merwilla plumbea plants grown for 4 weeks in perlite. Three different treatments were used: control (C); 1 mg Cd L⁻¹ (Cd1); and 5 mg Cd L⁻¹ (Cd5). Means ( ± s.e.) with different letters are significantly different (P < 0·05).

Fig. 3.

Effect of cadmium on dry weight of 17-week-old Merwilla plumbea plants grown for 4 weeks in perlite. Three different treatments were used: control (C); 1 mg Cd L⁻¹ (Cd1); and 5 mg Cd L⁻¹ (Cd5). Means ( ± s.e.) with different letters are significantly different (P < 0·05).

Fig. 4.

Effect of cadmium on cumulative leaf and root length of 17-week-old Merwilla plumbea plant grown for 4 weeks in perlite. Three different treatments were used: control (C); 1 mg Cd L⁻¹ (Cd1); and 5 mg Cd L⁻¹ (Cd5). Means ( ± s.e.) with different letters are significantly different (P < 0·05).

Fig. 5.

Effect of cadmium on average leaf and root length of 17-week-old Merwilla plumbea plants grown for 4 weeks in perlite. Three different treatments were used: control (C); 1 mg Cd L⁻¹ (Cd1); and 5 mg Cd L⁻¹ (Cd5). Means ( ± s.e.) with different letters are significantly different (P < 0·05).

Fig. 6.

Effect of cadmium application on cadmium concentration in roots, bulbs and leaves of 17-week-old Merwilla plumbea plants grown for 4 weeks in perlite. Three different treatments were used: control (C); 1 mg Cd L⁻¹ (Cd1); and 5 mg Cd L⁻¹ (Cd5). Means ( ± s.e.) with different letters are significantly different (P < 0·05).

Fig. 7.

Cross-sections of adventitious roots of Merwilla plumbea. Plants were grown in control conditions in perlite (A–C) and treated with 5 mg kg⁻¹ Cd (D–F). Roots in control conditions exhibit the typical structure of monocotyledonous roots formed by single-layered epidermis and single-layered exodermis (A, B); exodermal cells develop suberin lamellae close to the root apex, as shown in C after Fluorol yellow 088 staining in fluorescence microscopy. After cadmium treatment the hypodermal periderm is formed in the peripheral cortical zone close to the root apex (D–F). Cork cambium produces cells by periclinal division (E); these become impregnated by suberin, as shown in F after Fluorol yellow 088 staining in fluorescence microscopy. The distances of sections from the root apex are 5 mm (A, B, D, E) and 30 mm (C, F). Abbreviations: ep, epidermis; ex, exodermis; me, mesodermis (mid-cortical layers); en, endodermis; cc, central cylinder; asterisks indicate periclinal divisions in cork cambium. Scale bars: (A, D) = 100 µm, (B, C, E, F) = 50 µm.

Fig. 8.

Cross-section of adventitious roots of an adult Merwilla plant growing in soil (Botanical Garden of University of KwaZulu-Natal, Pietermaritzburg, South Africa) stained with Fluorol yellow 088 in UV light. The formation of multiseriate cell layers with suberized cell walls (*) resembling typical periderm occurs after injury of the root surface. Scale bar = 100 µm.