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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).
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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 p...
Citations
... Salt stress represents a significant environmental constraint that can disrupt osmotic potential and ion levels in plants, ultimately inhibiting cellular metabolism [60] . In high-salt environments, plants have evolved various mechanisms to combat salt stress. ...
Soil salinity is a significant environmental challenge that adversely affects plant yield and quality. Zoysiagrass (Zoysia japonica), a member of the Gramineae family, is highly salt-tolerant, making it an excellent model for studying salt stress response mechanisms. We performed physiological and transcriptomic analyses on two contrasting Zoysiagrass germplasm accessions under high salt conditions. The salt-tolerant germplasm ST68 demonstrated superior growth phenotypes, higher chlorophyll and relative water content, greater photochemical efficiency, and lower relative electrolyte leakage and sodium ion content compared to the salt-sensitive germplasm SS9. Transcriptomic analysis revealed differential expression in pathways involved in photosynthesis, flavonoid biosynthesis, cell wall macromolecule catabolism, phosphate ion homeostasis, and reactive oxygen species response in the tolerant vs the sensitive line under salt stress. Notably, the ZjHEMA gene, which encodes glutamyl-tRNA reductase, a rate-limiting enzyme in chlorophyll biosynthesis, was identified as a key regulator due to its significant upregulation under salt stress in the salt-tolerant germplasm, compared to the sensitive one. Overexpression of the salt-responsive glutamyl-tRNA reductase gene, associated with chlorophyll metabolism in Zoysiagrass, in Arabidopsis led to increased salt tolerance, as evidenced by elevated chlorophyll content, relative water content, and photochemical efficiency compared to wild-type plants. Our findings offer new insights into the mechanisms of salt tolerance in Zoysiagrass, laying a foundation for breeding salt-tolerant germplasm.
... Despite salt glands derived from within the epidermis, the structure and mechanistic approach toward salt excretion is different in recretohalophytes and other halophytes. Structurally, salt glands are grouped based on four types: salt bladders, multi-cell-based salt glands, bi-cell-based salt glands, and single-celled vacuolated secretory hairs (Dassanayake and Larkin 2017). Despite the types of salt glands found in halophytes, the typical gland has multiple cells ranging between 4 and 40 cells. ...
The book chapter elucidates the sophisticated relationship between salt-tolerant halophytes and their microbiomes, shedding light on the biological and ecological aspects of this association within the scope of adaptability and climate change. The chapter further highlights the mechanisms through which the halophytes have evolved to thrive in saline environments, showcasing their unique features and adaptations at different levels. It also describes the utilization of halophytes in agriculture, food, forage, and pharmaceutical industries due to their ability to grow in extreme environments.
The chapter also addresses the consequences of climatic changes by referring to some studies. Based on the unique characteristics of halophytes, their use for preserving freshwater and restoring degraded land is also described. Overall, the book chapter contributes to the understanding of the significance of halophytes in our ecosystem, their interactions with microbiome, their possible utilization for multiple applications, and their mitigation with climate change.
... Salt-secreting mangroves have evolved epidermal glands to exclude salt from leaves by a mechanism that is poorly understood (Flowers and Colmer, 2015;Dassanayake and Larkin, 2017). ...
... Salt glands of A. marina are multicellular, consisting of two to four basal collecting cells, one or two disc-like, cutinised stalk cells and eight to twelve radially arranged secretory cells. A cuticular envelope completely encloses the salt glands, while an expanded cuticular chamber is present above the secretory cells (Dassanayake and Larkin, 2017). ...
... In the gland, the ions are transported in vesicles to the cap and secretory cells. The ions are secreted out of the glands via pores at the top, probably as a result of hydrostatic pressure (Dassanayake and Larkin, 2017;Lu et al., 2021). Salt secretion is an active process requiring energy, and the dominant ions secreted are Na + and Cl À . ...
The effects of salinity on the structure of salt glands and salt secretion were determined by comparing adult Avicennia marina trees growing in the field at two contrasting salinities: seawater and hypersalinity. Electron microscopy was used to determine gland frequency and ultrastructure. Ecophysiological measurements included ion analyses of soils and leaves, soil and xylem water potentials and photosynthesis. In the hypersalinity site, salt gland frequency was 47% lower than that at seawater conditions. Salt glands in the hypersalinity site were sunken within crypts, partially collapsed, degenerated, and covered with salt crystals. In the hypersalinity site, salt secretion during the day was lower than that in the seawater site by 33% ( p < 0.05), while there were no differences in night secretion. In both sites, salt secretion was higher at night and lower during the day. In the hypersalinity site, the cytoplasm of the salt glands had fewer ribosomes and mitochondria and larger vacuolar and vesicular volume than at the seawater site. CO 2 exchange, conductance, transpiration and intrinsic Photosystem II efficiency. were significantly lower in the hypersalinity site than in the seawater site. Lower salt secretion in the hypersalinity site was probably due to lower salt gland frequency induced by xeromorphic characteristics such as smaller, thicker leaves, lower specific area, and thicker cuticles. The ecophysiological data supported the ultrastructural evidence that salt secretion is compromised by prolonged hypersalinity in adult Avicennia marina trees.
... Salt glands can effectively regulate the salt balance in plants and reduce the impact of salt stress on plants by actively excreting salt [70]. However, although the physiological differences between mangrove species with and without salt glands have been extensively studied [71][72][73], the identity and functional differences of leaf surface microorganisms of these two types of mangrove species have not been fully studied. ...
Background:
Mangrove plants growing in the high salt environment of coastal intertidal zones colonize a variety of microorganisms in the phyllosphere, which have potential salt-tolerant and growth-promoting effects. However, the characteristics of microbial communities in the phyllosphere of mangrove species with and without salt glands and the differences between them remain unknown, and the exploration and the agricultural utilization of functional microbial resources from the leaves of mangrove plants are insufficient.
Results:
In this study, we examined six typical mangrove species to unravel the differences in the diversity and structure of phyllosphere microbial communities between mangrove species with or without salt glands. Our results showed that a combination of salt-tolerant growth-promoting strains of Pantoea stewartii A and Bacillus marisflavi Y25 (A + Y25) was constructed from the phyllosphere of mangrove plants, which demonstrated an ability to modulate osmotic substances in rice and regulate the expression of salt-resistance-associated genes. Further metagenomic analysis revealed that exogenous inoculation with A + Y25 increased the rice rhizosphere's specific microbial taxon Chloroflexi, thereby elevating microbial community quorum sensing and ultimately enhancing ionic balance and overall microbial community function to aid salt resistance in rice.
Conclusions:
This study advances our understanding of the mutualistic and symbiotic relationships between mangrove species and their phyllosphere microbial communities. It offers a paradigm for exploring agricultural beneficial microbial resources from mangrove leaves and providing the potential for applying the salt-tolerant bacterial consortium to enhance crop adaptability in saline-alkaline land. Video Abstract.
... (i) The formation in the leaves of specialized excretory structures called saliferous glands or trichomes with four distinct types of structure [125], which usually excrete ions (Na + , Cl − , Ca 2+ , Zn 2+ , Pb 2+ , Cu 2+ ). (ii) The synthesis of heavy metal-chelating macromolecules (PCs and metallothioneins, and polyphosphates). ...
Osmoregulation mechanisms are engaged in the detoxification and accumulation of heavy metals in plants, microalgae and other microorganisms. The present review paper analyzes osmotic resistance organisms and their heavy metal accumulation mechanisms closely related to osmoregulation. In prokaryotic and eukaryotic microorganisms, such as the green algae-like protist Euglena, osmotic and heavy metal stresses share similar cell responses and mechanisms. Likewise, some plants have developed specific mechanisms associated to water stress induced by salinity, flooding, or drought, which are also activated under heavy metal stress. Thus, synthesis of osmo-metabolites and strategies to maintain stable the intracellular water content under heavy metal exposure induce a state of apparent drought by blocking the water maintenance systems. Heavy metals affect the cellular redox state, triggering signaling pathways for intracellular water maintenance, which are mediated by the concentration of reactive oxygen species. Hence, cellular responses and mechanisms associated with osmotic stress, once fully elucidated, represent new opportunities to improve mechanistic strategies for bioremediation of heavy metal-polluted sites.
... These have single large bladder cell at the top and a stalk consisting of one or more than one cells (Barkla and Vera-Estrella 2015). Another type of salt secretory glands is multicellular salt gland, which have been reported in numerous flowering families of desert and coastal areas such as Poaceae, Avicenniaceae, Acanthaceae, Plumbaginaceae, and Tamaricaceae (Dassanayake and Larkin 2017). These are prominent and elaborated structures on leaves. ...
Naturally adapted populations of a leafy succulent desert halophyte Salsola imbricata were evaluated for growth patterns, and, structural and functional modifications, that ensures their success in highly salt-affected habitats. The populations were collected from five diverse habitats least saline (DWF-Derawar Fort), moderately saline (TWT-Trawaywala Toba and BWD-Bailahwala Dahar), and highly saline (LAS-LadamSir and PAS-Pati Sir) along with rhizospheric soil samples. All population showed very specific modifications, i.e., increased root cross-sectional area, epidermal and endodermal thickness, sclerification in cortical and stellar region, proportion of storage parenchyma, and widened metaxylem vessels at root level. Decreased phloem area, pith thickness, and cell area and increased stem cross-sectional area, epidermal thickness, sclerifica-tion in vascular bundles, cortical region thickness, and enlarge metaxylem vessels was recorded in stems. Leaf modifications included increased leaf thickness due to thickened midrib, lamina, epidermis and cortical cells. Contrarily, much reduced vascular bundles, mainly the phloem region, decreased mesophyll thickness, and narrow xylem vessels were observed in leaves. The populations inhabiting highly saline environment showed better growth, salt exclusion, internal structural, and increased uptake of Na + , K + , and Ca 2+ in roots and shoots. These strategies of S. imbricata seemed to be evolutionary, which may be evolved in response to environmental adversities over long spanning period.
... These specialised secretory structures primarily serve to expel salt solutes from tissues when the soil's salt concentration exceeds the plant's tolerance levels [43]. This adaptation is typical for halophytes-plants that grow in saline soils [44]. Importantly, the multi-ionic solutes excreted onto the leaf surface undergo crystallisation and form conglomerates of minuscule crystals (Figure 1b) [17]. ...
Plants are able to produce various types of crystals through metabolic processes, serving functions ranging from herbivore deterrence to photosynthetic efficiency. However, the structural analysis of these crystals has remained challenging due to their small and often imperfect nature, which renders traditional X-ray diffraction techniques unsuitable. This study explores the use of Microcrystal Electron Diffraction (microED) as a novel method for the structural analysis of plant-derived microcrystals, focusing on Armeria maritima (Milld.), a halophytic plant known for its biomineralisation capabilities. In this study, A. maritima plants were cultivated under controlled laboratory conditions with exposure to cadmium and thallium to induce the formation of crystalline deposits on their leaf surfaces. These deposits were analysed using microED, revealing the presence of sodium chloride (halite), sodium sulphate (thénardite), and calcium sulphate dihydrate (gypsum). Our findings highlight the potential of microED as a versatile tool in plant science, capable of providing detailed structural insights into biomineralisation processes, even from minimal and imperfect crystalline samples. The application of microED in this context not only advances the present understanding of A. maritima’s adaptation to saline environments but also opens new avenues for exploring the structural chemistry of biomineralisation in other plant species. Our study advocates for the broader adoption of microED in botanical research, especially when dealing with challenging crystallographic problems.
... This suggests that salt glands may have been ruptured by the emergence of salt crystals which appeared at high concentrations as observed in Sporobolus virginicus [22]. The disappearance of salt glands and observation of salt crystals on the leaf surface of Wild cabbage under higher concentrations is a clear indication of ion secretion, which implies that the plant can be categorized under halophytes that are salt secretors (exo-recretohalophytes) [21,23,24]. This is supported by reports suggesting that certain halophytes (recretohalophytes) could excrete excess salt as a liquid that crystallizes and appears apparent on the surface of plant Table 2. Main chemical components detected on the surface and subsurface of leaves using energy dispersive spectroscopic analysis ...
... Plants have various strategies to cope with salt stress, involving refinement in their cellular physiology, phenotypic structures, osmoregulation, antioxidant production, and the regulation of signaling pathways (Van Zelm et al., 2020;Zhao et al., 2020). For instance, plants eliminate excess salt through a salt excretion mechanism to minimize salt-damage (Dassanayake and Larkin, 2017). Plants can also modify their root structure, such as developing deeper root systems to increase water uptake and mitigate the impact of salinity (Galvan-Ampudia and Testerink, 2011). ...
Soil salinization poses a critical problem, adversely affecting plant development and sustainable agriculture. Plants can produce soil legacy effects through interactions with the soil environments. Salt tolerance of plants in saline soils is not only determined by their own stress tolerance but is also closely related to soil legacy effects. Creating positive soil legacy effects for crops, thereby alleviating crop salt stress, presents a new perspective for improving soil conditions and increasing productivity in saline farmlands. Firstly, the formation and role of soil legacy effects in natural ecosystems are summarized. Then, the processes by which plants and soil microbial assistance respond to salt stress are outlined, as well as the potential soil legacy effects they may produce. Using this as a foundation, proposed the application of salt tolerance mechanisms related to soil legacy effects in natural ecosystems to saline farmlands production. One aspect involves leveraging the soil legacy effects created by plants to cope with salt stress, including the direct use of halophytes and salt-tolerant crops and the design of cropping patterns with the specific crop functional groups. Another aspect focuses on the utilization of soil legacy effects created synergistically by soil microorganisms. This includes the inoculation of specific strains, functional microbiota, entire soil which legacy with beneficial microorganisms and tolerant substances, as well as the application of novel technologies such as direct use of rhizosphere secretions or microbial transmission mechanisms. These approaches capitalize on the characteristics of beneficial microorganisms to help crops against salinity. Consequently, we concluded that by the screening suitable salt-tolerant crops, the development rational cropping patterns, and the inoculation of safe functional soils, positive soil legacy effects could be created to enhance crop salt tolerance. It could also improve the practical significance of soil legacy effects in the application of saline farmlands.
... With loss of Ca 2+ , selective transport of Ca 2+ to salt glands requires increases in energy consumption (Dassanayake and Larkin, 2017). Under control conditions, tetraploids decreased the allocation of Ca 2+ to salt glands, thereby reducing the energy expenditure for transport and retaining more Ca 2+ in leaf mesophyll cells as essential nutrients and signaling molecules for normal plant growth and metabolism (Dayod et al., 2010). ...
Under salt stress, recretohalophyte Plumbago auriculata tetraploids enhance salt tolerance by increasing selective secretion of Na⁺ compared with that in diploids, although the mechanism is unclear. Using non-invasive micro-test technology, the effect of salt gland Ca²⁺ content on Na⁺ and K⁺ secretion were investigated in diploid and tetraploid P. auriculata under salt stress. Salt gland Ca²⁺ content and secretion rates of Na⁺ and K⁺ were higher in tetraploids than in diploids under salt stress. Addition of exogenous Ca²⁺ increased the Ca²⁺ content of the salt gland in diploids and is accompanied by an increase in the rate of Na⁺ and K⁺ secretion. With addition of a Ca²⁺ channel inhibitor, diploid salt glands retained large amounts of Ca²⁺, leading to higher Ca²⁺ content and Na⁺ secretion rate than those of tetraploids. Inhibiting H2O2 generation and H⁺-ATPase activity altered Na⁺ and K⁺ secretion rates in diploids and tetraploids under salt stress, indicating involvement in regulating Na⁺ and K⁺ secretion. Our results indicate that the increased Na⁺ secretion rate of salt gland in tetraploids under salt stress was associated with elevated Ca²⁺ content in salt gland.
