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.

The elemental composition of halophytes correlates with key morphological adaptations and taxonomic groups

“…Salts accumulated in these trichomes are deposited on the leaf surface when trichomes collapse, and subsequently washed off the plants by rain, wind or gravity (Abdelly et al, 2008;Albert, 1975;Lambers et al, 2008;Schirmer and Breckle, 1982). Salt glands are special appendages within epidermal cell layer that actively secrete salts out of the leaves (Dassanayake and Larkin, 2017a;Duarte et al, 2015;Grattan and Grieve, 1992;Lambers et al, 2008;Zedler et al, 2003;Zoerb et al, 2013). Eu-halophytes also include some succulent plants, which accumulate high Na and Cl in their photosynthetic tissues by the absorption of extra water in their vacuoles.…”

Revealing mechanisms of salinity tissue tolerance in succulent halophytes: A case study for Carpobrotus rossi

“…As a result, all modern crops are sensitive to salinity. Until now, all attempts to improve salinity stress tolerance of crops has met only with a limited success (Dassanayake & Larkin, ; Flowers & Colmer, ; Mickelbart, Hasegawa, & Bailey‐Serres, ; Polle & Chen, ). At the same time, the problem of land salinization is only going to increase in a future, first as a result of a more intensive use of a poor quality irrigation water, and second, due to a need to expand agricultural food production into marginal lands, to match the population growth.…”

“…Halophytes represent only about 1% of all terrestrial plants but can thrive under conditions that would kill majority of conventional crops. Mechanisms of salinity tolerance in halophytes have been a subject of many comprehensive reviews in the last decade (Bose, Rodrigomoreno, & Shabala, ; Dassanayake & Larkin, ; Flowers & Colmer, ; Flowers, Munns, & Colmer, ; Mishra & Tanna, ; Ozfidan‐Konakci et al, ; Rozema & Schat, ; Shabala & Mackay, ; Shabala, Bose, & Hedrich, ; Volkov, ). All authors are at consensus that the key trait that differentiates halophytes from glycophytes is the ability of the former for an efficient sequestration of the load away from the metabolically active tissues.…”

“…All authors are at consensus that the key trait that differentiates halophytes from glycophytes is the ability of the former for an efficient sequestration of the load away from the metabolically active tissues. This is achieved by either a regular secreting the excessive amounts of salt via specialized salt glands (Dassanayake & Larkin, ; Yuan, Leng, & Wang, ) or by depositing it into external (epidermal bladder cells, EBC; Kiani‐Pouya et al, ) or internal (storage vacuoles) structures (Bonales‐Alatorre et al, ; Shabala et al, ). Amongst these mechanisms, salt sequestration in EBC is the most studied, both at physiological and molecular levels (Agarie et al, ; Barkla, Veraestrella, & Raymond, ; Hariadi, Marandon, Tian, Jacobsen, & Shabala, ; Oh et al, ; Shabala et al, ; Zou et al, ).…”

“…secreting the excessive amounts of salt via specialized salt glands (Dassanayake & Larkin, 2017;Yuan, Leng, & Wang, 2016) or by depositing it into external (epidermal bladder cells, EBC; Kiani-Pouya et al, 2017) or internal (storage vacuoles) structures Shabala et al, 2014). Amongst these mechanisms, salt sequestration in EBC is the most studied, both at physiological and molecular levels (Agarie et al, 2007;Barkla, Veraestrella, & Raymond, 2016;Hariadi, Marandon, Tian, Jacobsen, & Shabala, 2011;Oh et al, 2015;Shabala et al, 2012;Zou et al, 2017).…”