Micro-Evolutionary Processes in Armeria maritima at Metalliferous Sites

Abstract

Tolerance to heavy metals in plants is a model process used to study adaptations to extremely unfavorable environments. One species capable of colonizing areas with high contents of heavy metals is Armeria maritima (Mill.) Wild. A. maritima plants growing in metalliferous areas differ in their morphological features and tolerance levels to heavy metals compared to individuals of the same species growing in non-metalliferous areas. The A. maritima adaptations to heavy metals occur at the organismal, tissue, and cellular levels (e.g., the retention of metals in roots, enrichment of the oldest leaves with metals, accumulation of metals in trichomes, and excretion of metals by salt glands of leaf epidermis). This species also undergoes physiological and biochemical adaptations (e.g., the accumulation of metals in vacuoles of the root's tannic cells and secretion of such compounds as glutathione, organic acids, or HSP17). This work reviews the current knowledge on A. maritima adaptations to heavy metals occurring in zinc-lead waste heaps and the species' genetic variation from exposure to such habitats. A. maritima is an excellent example of microevolution processes in plants inhabiting anthropogenically changed areas.

Keywords: Armeria maritima (Mill.) Willd; heavy metals; metalliferous areas; metallophyte; microevolution.

Figure 1

The appearance of A. maritima plants from the area near Warsaw (Poland), not contaminated with heavy metals: (a) habitat of the whole plant; (b) inflorescence with developed flowers; (c) seeds in calyxes. All photos by Olga Bemowska-Kałabun.

Figure 2

Leaf area of A. maritima after four months of culture in medium supplemented with 20 mM lead nitrate: (a) crystals on the leaf, magnification 25×; (b) salt glands among the cells of the epidermis cells; scanning electron microscope, magnification 2000×. Abbreviations: C—salt crystal; Gc—cells of the gland; Gsc—secretory cells of the gland; Sg—salt gland. All photos by Agnieszka Abratowska (based on Abratowska et al., 2015 [47], modified).

Figure 3

Morphological diversity of A. maritima plants grown in a greenhouse (generation F1) from seeds collected in metalliferous (1—zinc–lead slag heap from Plombières in Belgium; 2—zinc–lead waste heap from Bolesław in Poland) and non-metalliferous areas (3—meadow from northern Poland; 4—meadow from southern Poland). (a) The appearance of the whole plant. There are visible differences in the lengths of the generative shoots of plants from individual populations. Plants from metalliferous areas (1, 2) have shorter shoots than those from non-metalliferous areas (3, 4). (b) Inflorescence buds, where in plants from metalliferous areas (1, 2), the length of the outer involucral bracts of the inflorescence bud does not exceed the length of the bud (black arrows), while in plants from non-metalliferous areas (3, 4), it is twice as long as the bud (black arrows). All photos by Agnieszka Abratowska (based on Abratowska et al., 2015 [47], modified).

Figure 4

The unrooted neighbor-joining (NJ) trees based on AFLP data: (a) a KpnI⁄MseI methylation-insensitive enzyme combination and (b) Acc65I/MseI methylation-sensitive enzyme combination from 136 individuals of A. maritima from two metalliferous populations—a zinc–lead waste heap from Bolesław in Poland (red oval) and a zinc–lead slag heap from Plombières in Belgium—as well as one non-metalliferous population—Manasterz in Poland (dry and semi-dry meadow). The numbers above branches denote bootstrap values, with Nei and Li’s genetic distances (based on Abratowska et al., 2012 [23], modified).