Plant Cell Rep. 29, 617–627. We examined the salt glands as putative salt and water bi-regulatory units that can respond swiftly to altering environmental cues. Salt uptake, signaling, transport, detoxification, and storage mechanisms are among the integral biological processes we need to understand in solving the puzzle of salt adaptation (see reviews Hasegawa et al., 2000; Deinlein et al., 2014). Plant Sci. Many factors influence salt secretion; for example, both the salt secretion ability and the density of salt glands of Glaux maritima L. increased under salt stress [27]. Salt glands on leaves of rhodes grass (Chloris gayana Kth.). Plant Cell. Tobacco NtLTP 1, a glandular-specific lipid transfer protein, is required for lipid secretion from glandular trichomes. (2016). 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, 2015). 11, 274–280. The ultrastructure of Frankenia salt glands. Song J, Wang BS. These results indicate that melatonin improves the salt tolerance of the recretohalophyte L. bicolor via the upregulation of salt secretion by the salt glands. Bot. No use, distribution or reproduction is permitted which does not comply with these terms. Waterlogging and salinity effects on two Suaeda salsa populations. 32, 459–469. BMC Genomics 16:605. doi: 10.1186/s12864-015-1813-9, Yasui, Y., Hirakawa, H., Oikawa, T., Toyoshima, M., Matsuzaki, C., Ueno, M., et al. Plant Sci. Correspondence to Impact Factor 4.402 | CiteScore 7.8More on impact ›, Salinity tolerance in plants: mechanisms and regulation of ion transport Proc. J. Exp. J. Mol. Exogenous melatonin increased the shoot dry weight of the seedlings exposed to 0 mM NaCl by 17.33%, whereas it increased the dry weight of the salt-treated seedlings by 20.9%. doi: 10.1016/S0367-2530(17)30346-8, Weiglin, C., and Winter, E. (1991). 73, 507–513. The Na+ and K+ contents were measured using a flame spectrophotometer (Model 2655–00 Digital Flame Analyzer; Cole-Parmer Instrument Company, Vernon Hills, Illinois, USA), and the Cl− content was measured using an ion chromatograph (ICS-1100 ion chromatograph; Thermo Fisher Scientific, Waltham, MA, USA), as described by Lin et al. BMC Plant Biol. Chen, Y., Zong, J., Tan, Z., Li, L., Hu, B., Chen, C., et al. The seeds were sown on well-washed river sand in plastic pots (16 cm in diameter; after the leaves emerged, the plants were watered with Hoagland’s nutrient solution), which were placed in a growth chamber with 600 μmol m− 2 s− 1 light (15-h day/9-h night photoperiod), a temperature of 25 ± 3 °C/22 ± 3 °C (day/night), and a relative humidity of 60/80% (day/night). Gene 404, 61–69. We also like to thank Kieu-Nga Tran for help with processing Figure 1 and John Johnson and Lauren Taylor for assistance with proofreading. in response to salinity, light intensity, and aeration. doi: 10.1534/genetics.166.3.1451, Morohashi, K., Zhao, M., Yang, M., Read, B., Lloyd, A., Lamb, R., et al. These multicellular glands typically have cell types differentiated into basal collecting cells and distal secretory cells (Faraday and Thomson, 1986b; Thomson et al., 1988). Tripp, E. A., and Fekadu, M. (2014). doi: 10.1016/j.ympev.2004.09.002, Shi, Y., Yan, X., Zhao, P., Yin, H., Zhao, X., Xiao, H., et al. The editor and reviewers' affiliations are the latest provided on their Loop research profiles and may not reflect their situation at the time of review. doi: 10.1007/s00468-010-0417-x, Park, J., Okita, T. W., and Edwards, G. E. (2009). 40, 681–686. doi: 10.1093/aob/mcu267, Flowers, T. J., Flowers, S. A., Hajibagheri, M. A., and Yeo, A. R. (1990). (2010). Fortunately, well-characterized promoters are now available for engineering cell type-specific expression in Arabidopsis roots. J. Linn. 47, 71–76. Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Dev. H. T. Chan (Yokohama: International Tropical Timber Organization). doi: 10.1016/S0367-2530(17)30323-7, Reis, C., Sajo, M. G., and Stehmann, J. R. (2002). (2009). 92, 43–54. In a number of cases, cuticular material extends down the sides of the secretory and/or the basal collecting cells. Arrows indicate salt glands. 4, 718–726. 48, 45–58. These salt glands are unicellular hairs (Type 4 in Figure 1). J. Bot. Halophyte and glycophyte salt tolerance at germination and the establishment of halophyte shrubs in saline environments. 30, 861–867. “Plant proton pumps: regulatory circuits involving H+-ATPase and H+-PPase,” in Transporters and Pumps in Plant Signaling, eds M. Geisler and K. Venema (Berlin: Springer), 39–64. doi: 10.1111/j.1365-3040.1978.tb00753.x, Maathuis, F. J. M. (2014). 101, 323–330. Plant Mol Biol. 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. A system for the transformation and regeneration of the recretohalophyte Limonium bicolor. In addition, this treatment reduced the content of Na+ and Cl− in leaves, but increased the K+ content. Nat. (2011). Bajwa VS, Shukla MR, Sherif SM, Murch SJ, Saxena PK. 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. Mapping fiber and yield QTLs with main, epistatic, and QTL × environment interaction effects in recombinant inbred lines of upland cotton. Melatonin regulates plant growth and development [33,34,35], and plays an important role in plant resistance to stresses, especially salt stress [31], drought stress [36], cold stress [37], oxidation stress [38, 39], and nutrient deficiencies [40]. (2014). Salt glands of Armeria canescens (Host) Boiss: morphological and functional aspects. Pistil drip following pollination: a simple in planta Agrobacterium-mediated transformation in cotton. 4), promoting salt tolerance. doi: 10.1111/pce.12068, Tanaka, H., Hirakawa, H., Kosugi, S., Nakayama, S., Ono, A., Watanabe, A., et al. The melatonin content of L. bicolor leaves was quantified as described by Sun et al. For example, engineering potato or tomato could take advantage of substantial molecular resources that are already available. Limoniastrum monopetalum (L.) Boiss, a candidate plant for use in urban and suburban areas with adverse conditions. 19, 334–346. Protoplasma 240, 75–82. Transcriptomic analysis of a Tertiary relict plant, extreme xerophyte Reaumuria soongorica to identify genes related to drought adaptation. (2016). Recently, studies have indicated that the exogenous application of melatonin can improve the ion homeostasis of plants under salt stress by upregulating the expression of genes encoding NHX, SOS and other proteins with related functions [30, 51, 52]. 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., 1980). Given that there are several channels and transporters that can transport Na+ exclusively or together with other organic and inorganic ions in plant cells (reviewed in Maathuis, 2014; Maathuis et al., 2014), this process needs to be coordinated between multiple membrane systems to avoid futile cycling of Na+ and other ions including K+ or toxic accumulation of NaCl. 2002;14:465–77. K+ accumulation in the cytoplasm and nucleus of the salt gland cells of Limonium bicolor accompanies increased rates of salt secretion under NaCl treatment using NanoSIMS. An ecophysiological study of the salt secretion of four halophytes. Mishra, S., and Das, A. Effects of NaCl and melatonin on vesicle transport related genes LBVAMP721 (LB00297), LBVAP27 (LB11044) and LBVAMP121 (LB11277) expression in L. bicolor leaves in 6-wk-old seedlings at different time points after NaCl (300 mM) and melatonin (5 μM) treatment. Both the basal cell and the cap cell are cytoplasmically dense and rich in mitochondria, plastids, and vesicles. 6d), relative to the control. All authors read and approved the final manuscript. A., et al. and Aegialitis annulata Rbr. doi: 10.2135/cropsci1994.0011183X003400030020x, Grigore, M. N., Ivanescu, L., and Toma, C. (2014). Theor. New York: Academic Press; 1972. A first step would be attempting to engineer Arabidopsis trichomes to function as bladder cells. 138, 171–190. Morphology and ultrastructure of the salt glands on the leaf surface of Rhodes grass (Chloris gayanaKunth). Article  Following the 300 mM NaCl treatment, the expression levels of LbSOS1 were significantly upregulated after 24, 36, 48, and 72 h (Fig. J. Nanosci. Transcriptome analysis of smooth cordgrass (Spartina alterniflora Loisel), a monocot halophyte, reveals candidate genes involved in its adaptation to salinity. 19 DNA Res. Lett. Am. Characterization and fine mapping of the glabrous leaf and hull mutants (gl1) in rice (Oryza sativa L.). 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. doi: 10.1016/j.sajb.2013.06.007, Yuan, F., Chen, M., Yang, J., Leng, B., and Wang, B. Excretion of salt through salt glands in non-halophytes may represent a facultative trait in response to salt stress derived from halophytic ancestral traits. Acta Botanica Neerlandica. Cell Biol. Although few species of plants have salt glands, they are distributed among four major divisions of flowering plants: Caryophyllales, asterids, rosids, and Poaceae (Santos et al., 2016). (2015) and Yuan et al. Abstract. The ion transporters transport ions into the salt glands. doi: 10.1007/s00425-008-0878-y, Sengupta, S., and Majumder, A. L. (2010). doi: 10.1016/0092-8674(94)90118-X, Immelman, K. (1990). (2015). Development 125, 1161–1171. The availability of a reference genome for M. crystallinum will facilitate new comprehensive investigations of the critical role of salt glands in the survival of the whole plant under salt stress. The maize macrohairless1 locus specifically promotes leaf blade macrohair initiation and responds to factors regulating leaf identity. Environ. ), and Plumbaginaceae (Faraday and Thomson, 1986b) (e.g., Limonium, Aegialitis, and Limoniastrum), all of which are closely related families in Caryophyllales (Byng et al., 2016). Plant Physiol. Representative cellular organization of distinct salt gland structures found in angiosperms. 170, 28–36. 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. A BLAST search for homologous genes was carried out in both L. bicolor and other species, and homologous sequences were downloaded. doi: 10.1093/aob/mcu229, Budak, H., Kasap, Z., Shearman, R. C., Dweikat, I., Sezerman, U., and Mahmood, A. Plant Physiol. doi: 10.1111/j.1365-313X.2012.04888.x, Rozema, J., Gude, H., and Pollak, G. (1981). doi: 10.1007/s10529-009-0179-y. The continuous cuticle on the epidermis in some species thickens on top of the cap cell and forms a cuticular chamber that stores secreted salts as seen for some eudicot salt glands (Amarasinghe and Watson, 1988). 5:467. doi: 10.3389/fpls.2014.00467, Malcolm, C. V., Lindley, V. A., O’Leary, J. W., Runciman, H. V., and Barrett-Lennard, E. G. (2003). Advancing crop transformation in the era of genome editing. Variation in salt secretory activity of microhairs in grasses. Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis. Natl. Evelin H, Kapoor R, Giri B. Arbuscular mycorrhizal fungi inalleviation of salt stress: a review. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). doi: 10.1111/j.1365-3040.1989.tb01971.x, Marcum, K. B. 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. Transcriptome analysis of the holly mangrove Acanthus ilicifolius and its terrestrial relative, Acanthus leucostachyus, provides insights into adaptation to intertidal zones. A pretreatment with 5 μM melatonin significantly improved the growth of L. bicolor seedlings under 300 mM NaCl. RNA-seq analysis of the response of the halophyte, Mesembryanthemum crystallinum (ice plant) to high salinity. Development of the glands resembles that of the nonglandular hairs until the three-celled … doi: 10.1016/j.plantsci.2015.06.021, Ferreira de Carvalho, J., Poulain, J., Da Silva, C., Wincker, P., Michon-Coudouel, S., Dheilly, A., et al. 7:715. doi: 10.3389/fpls.2016.00715, Amarasinghe, V., and Watson, L. (1988). Glandular trichomes on vegetative and reproductive organs of Leonotis leonurus (Lamiaceæ). 32, 547–555. doi: 10.1080/11263504.2015.1027317, Santos, J., Al-Azzawi, M., Aronson, J., and Flowers, T. J. 6:873. doi: 10.3389/fpls.2015.00873, Volkov, V., Hachez, C., Moshelion, M., Draye, X., Chaumont, F., and Fricke, W. (2006). The structure of the salt gland of Aegiceras corniculatum. 2017;160:396–409. Only a few species reportedly have salt glands in the large rosid clade. Although salt glands appear to have originated independently at least 12 times, they share convergently evolved features that facilitate salt compartmentalization and excretion. Only about 0.25% of all flowering plants are reportedly able to complete their lifecycle in saline soils (Flowers et al., 2010) and are hence considered to be halophytes. Single cell-type comparative metabolomics of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum. Salt is partially excluded by the roots and the salt is excreted by the salt glands by the plant expending energy. 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. If exogenous melatonin increases the salt-secreting ability of recretohalophytes, whether it is by regulating the ion transporters and vesicular transport proteins. (2015). Thomson WW, Liu LL. J. Exp. Identification of novel and conserved miRNAs from extreme halophyte, Oryza coarctata, a wild relative of rice. The Tree of Life Web Project. The Botany of Mangroves. Yuan, F., Chen, M., Yang, J., and Wang, B. High levels of activity inferred for the plasma membrane H+-ATPase and the Na+/H+ antiporter to compartmentalize more Na+ into the apoplast or the vacuole were suggested as key transporters in extruding excess salt from the young cotton leaves. These results indicate that ion transport proteins participate in the salt secretion process in L. bicolor. Many halophytic plants have epidermal glands on their leaves and stems which secrete salt (M etcalfe and C halk, 1950).These glands have been considered efficient devices for the secretion of excess salt which accumulates in the tissue (H aberlandt, 1914; H elder, 1956; S cholander, 1968; S cholander et al., 1962; 1965; 1966). Available at: http://tolweb.org/Core_Eudicots/20714/2005.01.01, Somaru, R., Naidoo, Y., and Naidoo, G. (2002). Sci. J. The values are the average of five biological repeats ± standard deviation. (2016). This broad phylogenetic distribution suggests that salt glands have originated independently multiple times as previously proposed for halophyte origins (Flowers et al., 2010). Crit. Nature 505, 546–549. In Ficus formosana the salt glands near hydathodes get dropped as the leaf ages removing compartmentalized excess salts more efficiently (Chen and Chen, 2005). Manage cookies/Do not sell my data we use in the preference centre. From a structural perspective, all salt glands appear to be largely epidermal in origin and thus are in essence specialized trichomes (Esau, 1965). *Correspondence: Maheshi Dassanayake, maheshid@lsu.edu John C. Larkin, jlarkin@lsu.edu, Front. Front. TABLE 1. doi: 10.1016/j.tplants.2014.09.001, Shahbaz, M., Ashraf, M., Al-Qurainy, F., and Harris, P. J. C. (2012). The salt glands of mangroves such as Acanthus, Aegiceras, Aegialitis and Avicennia are a distinctive multicellular trichome, a glandular hair found on the upper leaf surface and much more densely in the abaxial indumentum. 1). The exogenous melatonin treatment significantly increased the endogenous melatonin content of the L. bicolor leaves, with increases of 97.5% in the 0 mM NaCl-treated plants and 19.1% in the 300 mM NaCl-treated plants. root transcriptome and identification of candidate unigenes related to early responses under salt stress. Since even halophytes cannot tolerate large amounts of Na+ and Cl− in their cytoplasm, they either compartmentalize excess ions into vacuoles or transport ions into different tissues to maintain cytoplasmic ion homeostasis [1, 48, 49]. Developmental and subcellular organization of single-cell C4 photosynthesis in Bienertia sinuspersici determined by large-scale proteomics and cDNA assembly from 454 DNA sequencing. Funct. doi: 10.1590/S1516-89132002000100010, Renner, T., and Specht, C. D. (2013). Expression analysis of nine small heat shock protein genes from Tamarix hispida in response to different abiotic stresses and abscisic acid treatment. Melatonin is a pleiotropic molecule that regulates plant growth and can alleviate environmental stress in plants. It is unclear whether exogenous melatonin can increase the salt tolerance of halophytes, particularly recretohalophytes, by enhancing salt secretion from the salt glands. Plant Cell Physiol. The scarcity of genetic, cellular, or biochemical research on salt glands could be due to their occurrence on diverse taxa in plant families that are ecologically important, but not economically valued as crops. One type of halophyte, the recretohalophytes, secrete excess salt from salt glands or salt bladders located mainly on their leaves, thereby ensuring a lower Na+ content in their shoots and avoiding the excessive accumulation of ions in their cells, which protects against salt-associated damage [9, 10]. Bot. doi: 10.1104/pp.001164, Fu, X., Huang, Y., Deng, S., Zhou, R., Yang, G., and Ni, X. 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. Rozema J, Riphagen I. Physiology and ecologic relevance of salt secretion by the salt gland of Glaux maritima L. Oecologia. Combining the results of the current study with previous research, we formulated a novel mechanism by which melatonin increases salt secretion in L. bicolor (Fig. Is Arabidopsis trichome development a suitable model for engineering bladder cell-like salt glands? “Saline tolerance physiology in grasses,” in Ecophysiology of High Salinity Tolerant Plants, eds M. A. Khan and D. J. Weber (Berlin: Springer), 157–172. 168, 439–447. The concentration of the secreted fluid is always high, several times as high as the maximum urine concentration in birds. The 5 μM melatonin treatment significantly upregulated the expression levels of LbSOS1 after 24, 36, 48, and 72 h (Fig. 38, 459–462. 61, 199–205. (2015). Plant Sci. 55, 649–657. doi: 10.1007/BF01247900, Hasegawa, P. M., Bressan, R. A., Zhu, J.-K., and Bohnert, H. J. On the upper leaf surface they are sunken in shallow pits, and on the lower surface they occur scattered among long nonglandular hairs composed of three or four cells. The control seedlings were treated with Hoagland’s nutrient solution only. 4a) and Cl− (Fig. The ultrastructure of the salt glands of Cynodon and Distichlis (Poaceae). Although somewhat similar to the salt-secreting glands of eudicots, the salt glands of grasses differ in three important ways. Soc. doi: 10.1105/tpc.16.00196, Amaradasa, B. S., and Amundsen, K. (2016). (2013) wherein it is inferred that the salt tolerance trait evolved more than 70 times independently in diverse grass lineages with multiple events of loss of trait in some genera. doi: 10.1093/oxfordjournals.aob.a087671, Tan, W. K., Lim, T. K., Loh, C. S., Kumar, P., and Lin, Q.