Progress in Studying Salt Secretion from the Salt Glands in Recretohalophytes: How Do Plants Secrete Salt?

Abstract

To survive in a saline environment, halophytes have evolved many strategies to resist salt stress. The salt glands of recretohalophytes are exceptional features for directly secreting salt out of a plant. Knowledge of the pathway(s) of salt secretion in relation to the function of salt glands may help us to change the salt-tolerance of crops and to cultivate the extensive saline lands that are available. Recently, ultrastructural studies of salt glands and the mechanism of salt secretion, particularly the candidate genes involved in salt secretion, have been illustrated in detail. In this review, we summarize current researches on salt gland structure, salt secretion mechanism and candidate genes involved, and provide an overview of the salt secretion pathway and the asymmetric ion transport of the salt gland. A new model recretohalophyte is also proposed.

Keywords: asymmetric ion and water transport; recretohalophyte; salt gland; salt secretion mechanism; salt stress.

FIGURE 1

The structure and Na⁺ secretion pathway of a salt bladder (A) and a salt gland (B). (A) The large balloon represents the typical structure of the salt bladder. Na⁺ can be transported into the balloon and released after bladder rupture. The representative plant is Atriplex centralasiatica. (B) The typical multi-cellular salt gland and the Na⁺ pathway. The representative plant is Limonium bicolor. The photographs in (B) are reproduced from Feng et al. (2014) and Yuan et al. (2015) with some modifications. SC, secretory cell; AC, accessory cell; IC, inner cup cell; OC, outer cup cell; MC, mesophyll cell; EC, epidermal cell.

FIGURE 2

The reported recretohalophytes possessing salt glands with different salt secretion ability. The numbers on the bars presented the species numbers of one family. Red, the species of these families showed strong salt secretion. Purple, there has been no report about the salt secretion in these families until now. Blue, majority of this family showed week salt secretion except Aeluropus, Sporobolus, and Spartina. The figures were drawn with reference to Zhou et al. (2001) and Zhao et al. (2002).

FIGURE 3

The salt secretion of the salt gland with a distinct salt crystals on the leaves of Distichlis spicata (A) and Limonium bicolor (B). The photograph in (A) was reproduced from Semenova et al. (2010). The leaf blades of D. spicata exhibited salt crystals on their leaf surfaces after the plants were incubated in 0.55 mM NaCl solution for 20–24 h under conditions that prevented the slightest air flow (Semenova et al., 2010). The photograph in (B) was reproduced from Feng et al. (2014). Leaves of L. bicolor that were treated with 200 mM NaCl displayed distinct salt crystals on the surface of leaves, and the salt secretion rate per single salt gland was 8 ng h^–1, which is equivalent to a 5 mg Na⁺ secretion from a single mature leaf within 24 h after it was treated with 92 mg NaCl (200 mM) per day.

FIGURE 4

The possible pathway of Na⁺ transport from the mesophyll to the salt gland, and the way in which Na⁺ is secreted out. Na⁺ is transported into the salt gland through the bottom penetration area, which is not covered with cuticles (1), and the plasmodesmata (2). In the salt gland, the ions can be directly transported into the intercellular space (3). The ions are wrapped in vesicles for transport from the cytosol to the plasma membrane and secreted out of the salt gland cells (4). Plasmodesmata play an important role in ion delivery among the salt gland component cells (5). Various ion transporters are widely involved in moving salt in (6) and out (7). H⁺-ATPase participated in salt secretion by establishing electric potential difference and proton motive force across plasma membrane (8). Water channels (e.g., PIP) also take part in all the processes as a medium for ion transport (9). The ions are eventually exuded from the secreting pores at the top of the salt gland due to high hydrostatic pressure (10). Ion transporters responsible for influx (dark blue) and efflux (red) are asymmetrically distributed in the plasma membrane of salt gland cells. PLAS, plasmodesmata; HKT1, high-affinity K⁺ transporter 1; CNGC, cyclic nucleotide-gated cation channel; NSCC, non-selective cationic channel; PIP, plasma membrane intrinsic protein; NHX, Na⁺/H⁺ antiporter; SOS1, Na⁺/H⁺ antiporter; CLC, chloride channel.