Which mangrove extrudes salt

Indeed, the salt glands of various families tend to greatly resemble the structure of secretory glands of related plants that lack salt glands. For example, both Acanthus and Avicennia have a short stalk composed of 1—2 cells bearing a globular head consisting of secretory cells Shimony et al. The Acanthaceae Lamiales salt glands also bear a strong resemblance to the glandular trichomes that secrete essential oils in the closely related Lamiaceae.

These trichomes have a basal cell embedded in the epidermis, a one or two celled stalk, and a globular head of secretory cells with a sub-cuticular space where oils containing volatile secondary metabolites accumulate. This structural feature is redolent to the cuticular chambers with salt on top of salt glands Werker et al.

Glandular trichomes are common among the other clades in asterids as well. For example, Solanaceae short stalked globular trichomes Type VI that secrete defensive proteins Shepherd et al. The non-core Caryophyllales families, Plumbaginaceae, Tamaricaceae and Frankeniaceae, are sister to a clade of mostly carnivorous plants consisting of the families Droseraceae, Drosophyllaceae, Nepanthaceae, Dioncophyllaceae, and Ancistrocladaceae, which have glands that secrete digestive enzymes and mucilage.

Although the carnivorous plants have a variety of elaborate glandular morphologies that show secretory as well as absorption functions, these are thought to be derived from an ancestral character state for glands that are very similar to the salt glands of Tamarix and Frankinia Cameron et al.

The digestive glands of Dionaea muscipula Venus fly-trap , which consist of two layers of secretory cells above a pair of stalk cells and several basal cells that are embedded in the epidermis, may be taken as an example close to the ancestral state Scala et al. Like the salt gland secretory cells of Tamarix , these secretory cells have projections of cell wall material that increase the surface area of the secretory cell plasma membrane.

The pattern of convergent evolution of the secretory-type salt glands Figure 1 , Type 2 described here, combined with the resemblance of these salt glands to other types of glands on closely related plants, and in conjunction with the overall low frequency of plants bearing salt glands, suggests that these Type 2 salt glands have evolved independently multiple times from a common type of multicellular secretory gland found widely throughout eudicots.

A similar trend is observed for salt glands in monocots. Liphschitz and Waisel previously have suggested a common halophytic ancestor for the Chloridoideae species with salt glands. The Chloridoideae-type bicellular glands that secrete salts are found in a number of species in Cynodonteae and Zoysieae, but not all grasses in these subclades are halophytes.

For example, the bicellular glands in Eleusine indica and Sporobolus elongatus in Cynodonteae and Zoysieae, respectively, do not secrete salts and are not known as halophytes even if they carry glands with the same ultrastructure shared with Cynodonteae and Zoysieae halophytes Amarasinghe and Watson, Interestingly, the glandular organization consisting of a basal and cap cell is not limited to the Chloridoideae species, but it is also observed in more than species in the sister clade of panicoid grasses includes sorghum and corn.

However, these lack the plasma membrane invaginations in the basal cell characteristic of the halophytes in Chloridoideae Amarasinghe and Watson, Although salt glands are generally associated with halophytes, several Spartina spp. This could be a derived trait from an ancestral halophytic lifestyle of Spartina from saltmarshes and also coincides with the view presented by Bennett et al.

Collectively, we see that the ubiquitous bicellular glands in grasses can differentiate to salt secreting glands, microhairs without secretions, or glands that secrete other substances.

The salt secretory unicellular hairs reported for Porteresia coarctata show close resemblance to microhairs found in cultivated rice both in Oryzoideae , but rice microhairs do not show salt secretory functions detectable at significant levels Flowers et al. Some convergent trends occur multiple times in subsets of eudicot and monocot recretohalophytes separated by large evolutionary distances, indicative of the selective pressures driving salt gland evolution. For example, cell wall projections resulting in an increase in plasma membrane surface area are seen in both the Poaceae Levering and Thomson, ; Amarasinghe and Watson, and in the Tamaricaceae-Frankeniaceae-Plumbaginaceae clade Campbell and Thomson, ; Faraday and Thomson, b , although in Poaceae these projections protrude into the basal cell, while in Caryophyllales the protrusions occur into the secreting cell.

Such wall protrusions are characteristic of a wide variety of transfer cells that are involved in the intercellular transport of solutes Gunning and Pate, In another common trend, secretory-type salt glands are often located in pits or depressions on the leaf surface Tamaricaceae, Frankeniaceae, Plumbaginaceae, Primulaceae, Acanthaceae, Combretaceae, and Poaceae.

Perhaps these depressions collect dew into which salts can be efficiently secreted. This trait may have been further developed in Nolana mollis Solanaceae salt glands that primarily secreted NaCl, where excreted salts were used to condense water from unsaturated atmospheres as an adaptation to retrieve water for survival in the Atacama Desert Mooney et al.

This may suggest a trait highlighting adaptations to extreme drought tolerance from a preadapted halophytic trait.

The density of salt glands is highly species specific. For example, salt gland density generally ranges from 20 to 50 salt glands mm -2 in leaves of Limonium and Zoysia species Ding et al. The structural integrity of the salt glands may also depend on soil salinity and leaf age. For instance, the abaxial peg-like salt hairs on Porteresia coarctata tend to burst with increasing soil salinity where the adaxial more elongated salt hairs increase in density Sengupta and Majumder, In Ficus formosana the salt glands near hydathodes get dropped as the leaf ages removing compartmentalized excess salts more efficiently Chen and Chen, The functional significance provided by salt glands also changes with leaf development.

NaCl sequestration capacity may be the most critical function of salt bladders in young leaves of Aizoaceae and Amaranthaceae halophytes Agarie et al. Other functions including providing a secondary epidermal layer to protect against water loss, UV stress, and also serving as reserves for ROS scavenging metabolites and organic osmoprotectants may contribute more to plant survival under abiotic stress as the leaf matures Adolf et al.

The corresponding increased rate of salt secretion as a response to increasing concentrations of soil NaCl is also observed for salt glands in other plant clades Marcum et al.

The maximum rate of salt secretion, however, is dependent on the species. Because salt glands represent only a small proportion of the cells on the leaves of salt gland-bearing plants, studies regarding the cellular physiology and molecular genetics of salt glands have been limited in the past.

However, new methods are increasing our ability to study the detailed function of salt glands at the cellular level. The most accessible salt glands for study until recently have been bladder cells. The salt tolerant extremophiles Mesembryanthemum crystallinum ice plant has been the focus of the greatest number of biochemical, physiological, and genetic studies among halophytes with salt glands.

Steudle et al. The critical role played by salt bladders in M. The remarkable salt and drought tolerance capacity exhibited by M. Additionally, the recent cell specific targeted transcriptome, proteome, and metabolome analyses have reported the type of genes, proteins, and metabolites expressed specifically in salt glands in M.

These studies have helped to establish the importance of salt glands and their distinct functions from other leaf cells in a model halophyte. With the recent cell type specific experiments, we know that epidermal bladder cells of M. A significant number of lineage-specific genes of unknown function in response to salt stress were detected in these bladder cells.

Some of the lineage specific transcripts are easily detected in the epidermal bladder cell transcriptomes at high expression levels, but appear to be expressed at low levels or are undetected in whole shoot transcriptomes, indicating the importance of studies of individual salt gland cell types Oh et al.

Genes specific to bladder cell function and development that were identified using a suppression subtractive hybridization library construction between wild type M. One such gene of unknown function detected via the comparison between wildtype and mutant plants was subsequently overexpressed in Arabidopsis , resulting in a phenotype with an increased number of trichomes on leaves, and this gene was inferred to regulate trichome initiation via regulating GL2 in the trichome development pathway Roeurn et al.

The availability of a reference genome for M. Chenopodium quinoa Amaranthaceae , is an emerging model halophyte and a seed crop with several salt tolerant cultivars adapted to salt levels that are as high as that of sea water Adolf et al.

Its genomic complexity and polyploid nature have made molecular genetic analyses of the genetic mechanisms underlying its salt tolerance traits challenging. However, the draft genome of C. Also, the genome of the closely related non-halophyte Beta vulgaris Amaranthaceae and additional transcriptomes of the halophytic but non-salt gland subspecies B. Recently, Limonium bicolor has been developed as a model for the study of secretory multicellular salt glands.

Transcriptomic analysis of developing Limonium bicolor leaves while monitoring salt gland developmental stages suggests that salt gland development might be regulated by transcription factors homologous to those regulating trichome development in Arabidopsis thaliana , however, this suggestion is based solely on correlated expression patterns and weakly documented evidence for orthology Yuan et al.

Yuan et al. Additionally, the same group has optimized gamma radiation mutagenesis to create large mutant populations of L. The efforts to create a molecular toolbox for forward and reverse genetics in order to study the multicellular salt gland functions in Limonium bicolor are exemplary, given its status as a non-model organism in plant genetics.

In a salt gland, when certain cells take up the role of absorbing salt from neighboring cells and intercellular spaces main function proposed for collecting cells, basal cells, an sub-basal cells found in Type 2 and 3 salt glands in Figure 1 , other cells in the gland would need to export salts secretory and cap cells in Type 2 and 3 glands from Figure 1.

Salt from collecting basal cells can also be bulk transported via vesicles that fuse to the plasma membranes of collecting and secretory cells or cap cells in grasses , releasing salt to the extracellular space. A few studies have looked into the significance of vesicle transport in delivery of NaCl to secretory cells or extracellular spaces cuticle lined chamber in most multicellular salt glands and bicellular glands in grasses.

These studies have reported the formation of extra vesicles and fusion with the plasma membrane between basal cells and mesophyll cells and also basal and secretory cells upon salt treatment Thomson and Liu, ; Shimony et al. Faraday and Thomson a reported ion efflux rates in Limonium perezii salt glands that were significantly higher than rates possible exclusively via transmembrane transport. Congruently, Yuan et al.

Vesicle-mediated NaCl transport may provide the energy efficiency required for transporting salts through the salt glands that may not be feasible via transmembrane ion channels alone. The fiber crop Gossypium hirsutum Malvaceae , although is not considered a halophyte, is among the crop species most adapted to salt stress, and some cultivars also develop functional salt glands Gossett et al. The availability of a reference genome, multiple large scale transcriptome datasets, genetic transformation techniques, and genetic diversity estimates for a large group of cultivars make G.

However, the role of salt glands in adapting to salt stress in cotton has not been explored much until recent work published by Peng et al.

Among the monocot recretohalophytes, studies on Spartina spp. In addition, the genus Spartina offers an interesting evolutionary context where one can study the relaxed selection on genes important in salt gland functions when salt glands do not provide a fitness advantage to species that occupy freshwater habitats. Freshwater species including S. The development of salt glands in the freshwater species may be a result of a recent speciation event from ancestral salt marsh species.

This provides an excellent set of plants with natural replicates for comparative genomics in search of salt gland associated genes and their recruitment driven by salt stress or loss of recruitment in the absence of the selection pressure. Salt gland specific transcriptomic, proteomic, or metabolic datasets as genetic resources are challenging to obtain, often due to the tight integration of salt glands in leaf or other photosynthetic tissue.

Table 1 lists all genome wide molecular studies reporting datasets from plants with salt glands available at present October Several of these studies provide RNAseq-based experiments that target tissues enriched in salt glands.

A few studies have focused on enrichment of salt gland cell types or isolation of exclusive salt gland populations. Due to the structural diversity of these species, a method optimized for one species is difficult to implement in others.

Barkla et al. This technique is able to provide clean cell specific sap, but is impractical for multicellular salt glands. Techniques developed using pressure probes and picoliter osmometers to measure water potential and osmotic potential in single plant cells reviewed in Fricke, often used in crop plants Malone et al.

The use of epidermal peels enriched in salt glands is an alternative solution, although this technique introduces molecular signatures of regular epidermal cells to the sample, as contaminants are difficult to avoid Tan et al. Use of enzymatic digestion and subsequent grinding of epidermal peels has also been shown to be effective in isolating mangrove salt glands devoid of neighboring epidermal cells Tan et al. However, enzymatic digestion adds a significant amount of time that may lower the feasibility of using salt glands isolated through such techniques to detect transcript profiles dependent on plant treatments and conditions.

Treating epidermal peels with clearing solutions and detecting salt glands based on their autofluorescence has been successfully demonstrated for Limonium and Avicennia in identifying the salt gland structure and organization, but this method too would not allow time-sensitive assessments of salt gland-specific transcripts or proteins Tan et al. Effective methods shown successful in capturing multicellular gland-specific transcripts do not exist for halophytes at present.

However, this can be attempted using current molecular techniques. For example, fluorescent tags labeling entire cells, nuclei, or polysomes allow capture of cell-type specific transcripts in model plants Mustroph et al. Creating targeted transgenic lines for non-model halophytes could be a greater challenge than optimizing methods for cell-type specific tagging. One may need to explore Agrobacterium -independent transformation techniques if certain recretohalophytes prove to be recalcitrant to widely used transformation protocols Altpeter et al.

Furthermore, such methods require the identification of salt gland-specific promoter sequences. Candidate promoters might be deduced from promoters functioning in glandular trichome gene expression of related plants Choi et al. Alternatively, physically isolating multicellular glandular structures before extracting the cell sap for RNA, protein, or metabolite profiling has been established using laser capture microdissection methods Olofsson et al.

Is Arabidopsis trichome development a suitable model for engineering bladder cell-like salt glands? Salt glands provide an end destination for excess salts, and understanding the function of these specialized structures may ultimately play a role in producing salt-tolerant crops.

Although the engineered expression of individual genes involved in salt tolerance has had some success in increasing salt tolerance in artificial situations, this has not translated to increased salt tolerance under field conditions Flowers and Colmer, ; Mickelbart et al. Salt tolerance under real-world conditions is likely to require careful attention to cell and tissue-type specific expression of multiple proteins involved in salt tolerance. As noted above, virtually all salt glands are similar in structure, and likely homologous, to the trichomes of closely related plants.

The trichomes of Arabidopsis thaliana are one of the most well-studied models for plant development at the cellular level, and it was recently suggested that knowledge from Arabidopsis trichome development could be used to guide the engineering of bladder cell-type salt glands in crop plants Shabala et al.

This is a striking proposal that deserves serious consideration. A first step would be attempting to engineer Arabidopsis trichomes to function as bladder cells. Many direct downstream targets of this transcription factor complex have been identified, and mutations and gene-expression manipulations are established that alter the density of trichomes on leaves, trichome cell shape, and cell wall properties.

A number of direct downstream target genes of the trichome development transcription complex are known, and several relatively trichome-specific promoters are noted, e. The putative transcription factor identified in wild type M. Interestingly, the GaMYB2 promoter directed GUS expression exclusively in glandular cells of glandular secreting trichomes in tobacco where different types of trichomes exist Shangguan et al.

This suggests that complex tissue specific signals may exist for trichome specific expression in different halophytes even when the genetic components are well described in the model species. This detailed knowledge of Arabidopsis trichome development, in combination with new large-scale gene assembly tools that aid in transferring whole pathways to plant genomes such as BioBrick, Golden Gate, and Gibson assembly methods reviewed in Patron, , suggest that attempting to modify Arabidopsis trichomes to function as salt glands may be feasible.

It should be noted that some of the key target proteins involved in the salt response may include multiple subunits from different polypeptides and therefore, multiple genes need to be coordinately expressed to get the desired level of expression of the holoenzyme.

Further refinements could be made by taking advantage of the knowledge that increased GL3 expression increases trichome density on leaves Payne et al. Thus, introducing a copy of GL3 under the control of an ABA-inducible, salt-responsive promoter would be expected to increase the number of bladder cell-modified trichomes on the leaf in response to salt stress.

Although the prospect of engineering trichomes of a non-halophyte into functional bladder cells is exciting, there are naturally some serious caveats. First, salt glands of any sort are only one line of defense against salt, and this is achieved via the sequestration of salt that has reached photosynthetic shoot tissues to ameliorate the effects.

Truly salt-tolerant plants are likely to require engineering of gene expression in multiple tissues. Much evidence indicates that for plants, the initial line of defense is to prevent the accumulation of salt in the roots in the first place reviewed in Flowers and Colmer, Fortunately, well-characterized promoters are now available for engineering cell type-specific expression in Arabidopsis roots. The incorporation of tissue-specificity through the use of tissue-specific promoters is still ultimately too simplistic and likely will fail to capture the dynamic nature of true halophyte responses to saline conditions.

The final caveat to this approach is that the engineering of bladder cell-type salt glands based on Arabidopsis trichomes as a model is likely to be limited phylogenetically to plants sharing the same trichome initiation regulatory network. While the transcription complex that regulates Arabidopsis trichome development is clearly homologous to the transcription factors that regulate anthocyanin biosynthesis in plants as distantly related as the grasses, it appears that asterids regulate trichome development via the MIXTA -like MYB proteins, which lack the ability to bind GL3-like bHLH proteins Payne et al.

Furthermore, expression of Antirrhinum MIXTA does not affect Arabidopsis trichome development, and expression of Arabidopsis trichome regulators in Nicotiana also does not affect trichome formation.

Thus, trichome development appears to be regulated independently in the rosids and the asterids. In this light, it is interesting to note that in Mesembryanthemum crystallinum , a putative ortholog of the trichome development gene GL2 , exhibits increased expression in bladder cells in response to salt Oh et al.

Both of these plants are in the Caryophyllales. Thus, among dicotyledonous crops, approaches to salt gland engineering based on Arabidopsis trichomes may be limited to crops in the rosids, such as Brassica spp.

More significant to the engineering of crop plants, the limited evidence to date on trichomes in the grasses gives no support for the involvement of any MYB, basic-helix-loop-helix, or WD-repeat proteins in trichome development.

In maize, the mutant macrohairless1 lacks the large single-celled trichomes known as macrohairs, but the gene product is not known Moose et al. In rice, mutants of glabrous leaf and hull1 gl1 lack both macrohairs and microhairs, two classes of unicellular trichomes, but do not affect the development of the glandular trichomes. Thus what we learn from manipulating Arabidopsis trichomes to function as salt glands may not be readily applied to some of our most important crops, although crops in the rosids include not only the Brassica spp.

If engineering multicellular salt glands into a crop prior to establishing a proof of concept protocol in Arabidopsis is envisioned, Solanaceae crops provide alternative candidates. For example, engineering potato or tomato could take advantage of substantial molecular resources that are already available.

These crops have reference genomes available for both the main commercial cultivars and also for more stress tolerant wild relatives Xu et al. Solanaceae crops also have cultivars more tolerant to moderate salt levels Shahbaz et al. The idea of converting a glandular trichome to a salt secreting trichome bypasses the need to engineer cellular structural features needed for liquid excretion.

Still, this endeavor requires the knowledge of coupling stress signaling and coordination of salt transport from roots to shoots and finally to the modified glandular trichomes at a metabolic energy cost or yield penalty applicable or tolerable for a crop species. If a cereal crop model is chosen for engineering salt glands, rice would naturally be a top candidate, given the genetic resources available for rice as the prominent monocot model.

This essential crop that feeds more than 3 billion people is being increasingly threatened by salinity stress caused by climate induced salt water intrusion, thus endangering the nutrition of the billions that consume rice. However, more targeted functional genomic studies have to be conducted to identify its trichome development pathway as discussed above.

Comparative transcriptome-based studies on Porteresia coarctata salt hairs can further facilitate identification of the candidate orthologous genes one would need to introduce to selected rice cultivars.

Alternatively, given the availability of genetic resources, including a reference genome, for sorghum, its relatively high capacity for abiotic stress tolerance as a C4 grass, and its phylogenetic proximity to almost all the grass species that are known to secrete salt through salt glands makes sorghum another attractive model for salt gland engineering in cereals Paterson et al.

It should be noted that all reported salt-secreting grasses also happen to be C4 grasses, with the exception of Porteresia Table 1. The bicellular microhairs in Zea mays that are not considered to be salt glands show an increase in microhair density on leaves in response to increasing soil salinity Ramadan and Flowers, This suggests the possibility of shared regulatory pathways in microhair initiation between salt secreting grasses and non-secretors.

Notably, Zea mays has a significant amount of genomic resources, optimized genetic engineering tools, diverse germplasm from wild relatives, and cell type specific metabolic data Liang et al.

Such factors, in conjunction with the importance as a major food and as a biofuel crop, make it another candidate for engineering salt hairs with significant secretion capacity upon problematic soil salt levels. Inarguably, a significant amount of functional, evolutionary, and comparative genomics studies need to be initiated to understand the organization and coordination of molecular networks that could transform a non-salt secreting species to a salt secreting plant. Salt-stress is a substantial challenge for agriculture in the 21st century.

One mechanism used by a wide variety of plants to deal with saline conditions is the use of epidermal salt glands that sequester or excrete salt. Salt glands have independently evolved likely twelve or more times and exist in at least four distinct morphological types. Despite these diverse origins, significant shared features due to convergent evolution give insight into the selective forces that have shaped their evolution and function.

Although salt glands are challenging to study at the cellular and molecular level, new resources and tools have begun to elucidate the mechanisms by which salt glands alleviate salt stress.

The time is now ripe to begin applying lessons from salt gland physiology to improving the salt tolerance of agricultural crops. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We like to thank the LSU Interlibrary Loan services for efficiently retrieving many publications unavailable electronically that were used for this review.

We thank the four reviewers whose critical comments helped improve this manuscript. Adair, L. Characterizing gene responses to drought stress in fourwing saltbush Atriplex canescens Pursh Nutt. Range Manag. Adam, P. The salt glands of Samolus repens. Google Scholar. Adams, P. Growth and development of Mesembryanthemum crystallinum Aizoaceae. New Phytol. Adolf, V. Salt tolerance mechanisms in quinoa Chenopodium quinoa Willd. Plant Soil , — Agarie, S.

Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum. Ahn, J. De novo transcriptome analysis to identify anthocyanin biosynthesis genes responsible for tissue-specific pigmentation in Zoysiagrass Zoysia japonica Steud.

Akhani, H. Bienertia sinuspersici Chenopodiaceae : a new species from southwest asia and discovery of a third terrestrial C4 plant without Kranz anatomy. Altpeter, F. Advancing crop transformation in the era of genome editing.

Plant Cell 28, — Amaradasa, B. Transcriptome profiling of buffalograss challenged with the leaf spot pathogen Curvularia inaequalis. Plant Sci.

Amarasinghe, V. Comparative ultrastructure of microhairs in grasses. Variation in salt secretory activity of microhairs in grasses. Plant Physiol. Atkinson, M. Salt regulation in the mangroves Rhizophora mucronata Lam. Aversano, R. The Solanum commersonii genome sequence provides insights into adaptation to stress conditions and genome evolution of wild potato relatives. Plant Cell 27, — Aymen, S.

Salt tolerance of the halophyte Limonium delicatulum is more associated with antioxidant enzyme activities than phenolic compounds. Plant Biol. Baisakh, N. Primary responses to salt stress in a halophyte, smooth cordgrass Spartina alterniflora Loisel. Balsamo, R. Ultrastructural features associated with secretion in the salt glands of Frankenia grandifolia Frankeniaceae and Avicennia germinans Avicenniaceae.

Barhoumi, Z. Ultrastructure of Aeluropus littoralis leaf salt glands under NaCl stress. Protoplasma , — Barkla, B. Single cell-type comparative metabolomics of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum.

Plant Science Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum. Proteomics 12, — Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify salt-responsive proteins. BMC Plant Biol. Bedre, R. Transcriptome analysis of smooth cordgrass Spartina alterniflora Loisel , a monocot halophyte, reveals candidate genes involved in its adaptation to salinity.

BMC Genomics Bennett, T. Repeated evolution of salt-tolerance in grasses. Bhogaonkar, P. Anatomical characterization of Lepidagathis cristata Willd. Bohnert, H. The ice plant cometh: lessons in abiotic stress tolerance. Plant Growth Regul. Bolger, A. The genome of the stress-tolerant wild tomato species Solanum pennellii.

Bonales-Alatorre, E. Reduced tonoplast FV and SV channels activity is essential for conferring salinity tolerance in a facultative halophyte, Chenopodium quinoa. Breckle, S. El Bassam, M. Dambroth, and B. Loughman Berlin: Springer , — Bromham, L. Macroevolutionary patterns of salt tolerance in angiosperms. Budak, H. Molecular characterization of cDNA encoding resistance gene-like sequences in Buchloe dactyloides. Evolution of Buchloe dactyloides based on cloning and sequencing of matK, rbcL, and cob genes from plastid and mitochondrial genomes.

Genome 48, — Butler, N. Generation and inheritance of targeted mutations in potato Solanum tuberosum L. Byng, J. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV.

Cameron, K. Molecular evidence for the common origin of snap-traps among carnivorous plants. Campbell, C. Salt gland anatomy in Tamarix penandra Tamaricaceae. Campbell, N. The ultrastructure of Frankenia salt glands. The apoplastic pathway of transport to salt glands. Cardale, S. The structure of the salt gland of Aegiceras corniculatum. Planta 99, — Salt glands in the Poaceae family and their relationship to salinity tolerance.

High-frequency, precise modification of the tomato genome. Genome Biol. Chen, C. Study on laminar hydathodes of Ficus formosana Moraceae I.

Morphology and ultrastructure. Chen, Y. Systematic mining of salt-tolerant genes in halophyte Zoysia matrella through cDNA expression library screening. Cheng, X. Gene expression involved in dark-induced leaf senescence in zoysiagrass Zoysia japonica. Plant Biotechnol. Chiang, C. Identification of ice plant Mesembryanthemum crystallinum L.

Choi, Y. Tobacco NtLTP 1, a glandular-specific lipid transfer protein, is required for lipid secretion from glandular trichomes. Plant J. Coles, N. Development and use of an expressed sequenced tag library in quinoa Chenopodium quinoa Willd. Cushman, J. Dang, Z. Transcriptomic profiling of the salt-stress response in the wild recretohalophyte Reaumuria trigyna. Daraban, I. Cell Biol. Das, S. On the ontogeny of stomata and glandular hairs in some Indian mangroves. Acta Bot. Deal, R. Deinlein, U.

Plant salt-tolerance mechanisms. Trends Plant Sci. Ding, F. Progress in mechanism of salt excretion in recretohalopytes. Dohm, J. The genome of the recently domesticated crop plant sugar beet Beta vulgaris. Nature , — Drennan, P. Ultrastructure of the salt glands of the mangrove, Avicennia marina Forssk. Planta , — Du, L. Evaluation and exploration of favorable QTL alleles for salt stress related traits in cotton cultivars G.

Dwivedi, S. Landrace germplasm for improving yield and abiotic stress adaptation. Esau, K. Plant Anatomy. Etalo, D. Spatially resolved plant metabolomics: some potentials and limitations of laser-ablation electrospray ionization mass spectrometry metabolite imaging.

Faraday, C. Morphometric analysis of Limonium salt glands in relation to ion efflux. Structural aspects of the salt glands of the Plumbaginaceae. Feng, Z. Ferreira de Carvalho, J. Transcriptome de novo assembly from next-generation sequencing and comparative analyses in the hexaploid salt marsh species Spartina maritima and Spartina alterniflora Poaceae. Heredity , — Flowers, T. Plant salt tolerance: adaptations in halophytes. Salt tolerance in the halophytic wild rice, Porteresia coarctata Tateoka.

Evolution of halophytes: multiple origins of salt tolerance in land plants. Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Francisco, A. Morphoanatomical description of leaves glands types in the white mangrove Laguncularia racemosa L. Gaertn f. Acta Microsc. Fricke, W. Cell turgor, osmotic pressure and water potential in the upper epidermis of barley leaves in relation to cell location and in response to NaCl and air humidity.

The biophysics of leaf growth in salt-stressed barley. A study at the cell level. Fu, X. Construction of a SSH library of Aegiceras corniculatum under salt stress and expression analysis of four transcripts. Fuglsang, A. Geisler and K.

Venema Berlin: Springer , 39— Gao, C. Expression profiles of 12 late embryogenesis abundant protein genes from Tamarix hispida in response to abiotic stress.

World J. Expression profiling of salinity-alkali stress responses by large-scale expressed sequence tag analysis in Tamarix hispida. Plant Mol. Garg, R. Deep transcriptome sequencing of wild halophyte rice, Porteresia coarctata , provides novel insights into the salinity and submergence tolerance factors.

DNA Res. Giuliani, C. Insight into the structure and chemistry of glandular trichomes of Labiatae, with emphasis on subfamily Lamioideae. Plant Syst. Glas, J. Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Gossett, D. Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci. Grigore, M. Halophytes: An Integrative Anatomical Study.

Cham: Springer, doi: Gu, L. Analysis of gene expression by ESTs from suppression subtractive hybridization library in Chenopodium album L. Gucci, R. Salinity tolerance in Phillyrea species. Gunning, B.

Protoplasma 68, — Hasegawa, P. Plant cellular and molecular responses to high salinity. Heubl, G. Molecular phylogeny and character evolution of carnivorous plant families in Caryophyllales - revisited.

Hu, L. RNA-seq for gene identification and transcript profiling in relation to root growth of bermudagrass Cynodon dactylon under salinity stress. Huang, J. Transcriptome sequencing and analysis of leaf tissue of Avicennia marina using the Illumina platform. Genetic dissection of trichome cell development in Arabidopsis.

Cell 76, — Immelman, K. Studies in the southern African species of Justicia and Siphonoglossa Acanthaceae : indumentum. Bothalia 20, 61— Ioannidou-Akoumianaki, A. Limoniastrum monopetalum L. Boiss, a candidate plant for use in urban and suburban areas with adverse conditions. An anatomical and histochemical study. IPCC Pachauri and L. Ismail, H.

Jakoby, M. Jou, Y. Vacuolar acidity, protein profile, and crystal composition of epidermal bladder cells of the halophyte Mesembryanthemum crystallinum. Jyothi-Prakash, P. Identification of salt gland-associated genes and characterization of a dehydrin from the salt secretor mangrove Avicennia officinalis. Karimi, S. Development of epidermal salt hairs in Atriplex triangularis Willd.

Gazette , 68— Khan, T. High-frequency regeneration via somatic embryogenesis of an elite recalcitrant cotton genotype Gossypium hirsutum L.

Plant Cell Tissue Organ. Kim, C. Transcriptome analysis of leaf tissue from Bermudagrass Cynodon dactylon using a normalised cDNA library.

Ko, S. Transcriptomic analysis of zoysiagrass using expressed sequence tags. Kortbeek, R. Kriegel, A. Larkin, J. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis.

Levering, C. The ultrastructure of the salt gland of Spartina foliosa. Planta 97, — Li, F. Genome sequence of cultivated Upland cotton Gossypium hirsutum TM-1 provides insights into genome evolution.

Li, J. Generation and analysis of expressed sequence tags ESTs from halophyte Atriplex canescens to explore salt-responsive related genes. Li, W. Characterization and fine mapping of the glabrous leaf and hull mutants gl1 in rice Oryza sativa L. Plant Cell Rep. Liang, Z. Lin, M. Global analysis of the Gossypium hirsutum L. Transcriptome during leaf senescence by RNA-Seq. Liphschitz, N. Salt glands on leaves of rhodes grass Chloris gayana Kth. Existence of salt glands in various genera of the Gramineae.

Liu, M. Analysis of differentially expressed genes under UV-B radiation in the desert plant Reaumuria soongorica. Gene , — Liu, Y. Identification of differentially expressed genes in leaf of Reaumuria soongorica under PEG-induced drought stress by digital gene expression profiling. Longstreth, D. Salinity effects on leaf anatomy: consequences for photosynthesis.

Membrane potentials and salt distribution in epidermal bladders and photosynthetic tissue of Mesembryanthemum crystallinum L. Plant Cell Environ. Maathuis, F. Sodium in plants: perception, signalling, and regulation of sodium fluxes. Photo taken on the mangrove walk St Kilda, South Australia. New findings of Distichlis spicata showed that these ions were transported into the salt gland through the bottom penetration area that was not covered by the cuticles of the salt gland, and the cuticles can prevent the ions from backflowing into the mesophyll Semenova et al.

Ions accumulated in the salt gland via the bottom penetration area and plasmodesmata generated fluid pressure due to the presence of the cuticle, and then secreted through salt gland pores. Dschida, K. Ion movement through the symplast to the secretory cells of the glands is probably diffusive and cell to cell via plasmodesmata [connecting channels] Fitzgerald and Allaway We note that this model has many similarities to hypothesis of ion transport across roots Hanson ; Clarkson , and there are strong similarities in the evidential bases for these, both structurally and physiologically.

Balsamo, Michael E. Adams and William W. By making their hairs stand up, numbats expose more skin to the sun and create an insulating layer of air to reduce heat loss. Aquaporin molecules form a channel that allows water to move across cell membranes. Hibernating hedgehogs slow their metabolism and organ function to a near standstill. The wing scales of a green birdwing butterfly help regulate body heat by using a honeycomb structure to enhance black pigments found in the wings.

We use cookies to give you the best browsing experience. By clicking the Accept button you agree to the terms of our privacy policy. Glands Remove Excess Salt Mangroves. Functions Performed More from this Living System. Maintain Homeostasis When a living system is in homeostasis, it means that internal conditions are stable and relatively constant.

See More of this Function. See More of this Living System. Mangrove in Jozani Forest, Zanzibar. Journal article Epidermal Peels of Avicennia germinans L. Thomson embedly preview toggle icon Reference toggle icon. Other Biological Strategies.

Term Definition toggle icon. Please go back and try again, or use the main menu above.