Making Plants Break a Sweat: the Structure, Function, and Evolution of Plant Salt Glands

Abstract

Salt stress is a complex trait that poses a grand challenge in developing new crops better adapted to saline environments. Some plants, called recretohalophytes, that have naturally evolved to secrete excess salts through salt glands, offer an underexplored genetic resource for examining how plant development, anatomy, and physiology integrate to prevent excess salt from building up to toxic levels in plant tissue. In this review we examine the structure and evolution of salt glands, salt gland-specific gene expression, and the possibility that all salt glands have originated via evolutionary modifications of trichomes. Salt secretion via salt glands is found in more than 50 species in 14 angiosperm families distributed in caryophyllales, asterids, rosids, and grasses. The salt glands of these distantly related clades can be grouped into four structural classes. Although salt glands appear to have originated independently at least 12 times, they share convergently evolved features that facilitate salt compartmentalization and excretion. We review the structural diversity and evolution of salt glands, major transporters and proteins associated with salt transport and secretion in halophytes, salt gland relevant gene expression regulation, and the prospect for using new genomic and transcriptomic tools in combination with information from model organisms to better understand how salt glands contribute to salt tolerance. Finally, we consider the prospects for using this knowledge to engineer salt glands to increase salt tolerance in model species, and ultimately in crops.

Keywords: convergent evolution; halophytes; salt glands; salt secretion; trichomes.

FIGURE 1

Representative cellular organization of distinct salt gland structures found in angiosperms. Drawings are based on consensus representations of species specific salt gland structures. References used to create consensus figures for each type are given in Table 1. The cells that constitute the salt gland are colored while the adjacent cells are kept blank. The continuous cuticle around the salt gland is also colored and changed to blank when the cuticle overlays the surrounding epidermis. The dynamic intracellular structures such as vacuoles, vesicles, and laminated membranes are not depicted in the representative figures. Collecting cell (Col), secretory cell (Sec), basal cell (BC), sub-basal cell (SBC), stalk cell (ST).

FIGURE 2

Phylogenetic distribution of angiosperm clades reported to have salt glands. Families associated with the four types of salt glands discussed in this review are grouped in the same colors used to distinguish salt gland types in Figure 1. The asterisk symbols (^∗) represent 12 likely independent introductions of salt glands into a family/clade. Phylogenetic relationships are based on the APG IV classification system (Byng et al., 2016).