Abstract
Salt stress is harmful to plants, especially for those that live under conditions of intense salt aport. For this reason, several species present alternatives to prevent or diminish the damages that high salt concentrations may cause to the cells. Salt glands are one of these alternatives once they are specialized structures that secrete salt. Here, we aimed to investigate if the glandular trichomes in the leaves of Jacquinia armillaris are salt glands. Anatomical and ultrastructural observations showed that the glandular trichomes in J. armillaris resemble the salt glands from other recretohalophytes Primulaceae, such as, their occurrence in sunken regions in the leaf epidermis, the presence of a large basal cell that acts as a collecting cell, the detachment of the cuticle from the outer periclinal walls forming a cuticular chamber, the thickness of the cuticle in the stalk portion of the trichome, and the presence of sodium and chloride ions in the secretion and in the xylem. Altogether, the gathered results support the hypothesis that the glandular trichomes in J. armillaris are adapted to salt secretion, thus characterizing as salt glands.
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References
Adam P, Wiecek BM (2010) The salt glands of Samolus repens. Wetlands Australia 3:2–11. https://doi.org/10.31646/wa.66
Aronson J, Pasternak D, Danon A (1988) Introduction and first evaluation of 120 halophytes under seawater irrigation. In: Whitehead EE, Hutchinson CF, Timmermann BN, Varady RG (eds) Arid lands: today and tomorrow. Westview, Boulder
Ascensão L (1998) The leaf capitate trichomes of Leonotis leonurus: histochemistry, ultrastructure and secretion. Ann Bot 81:263–271. https://doi.org/10.1006/anbo.1997.0550
Balsamo RA, Thomson WW (1993) Ultrastructural features associated with secretion in the salt glands of Frankenia grandifolia (Frankeniaceae) and Avicennia germinans (Avicenniaceae). Am J Bot 80:1276–1283. https://doi.org/10.2307/2445711
Barhoumi Z, Djebali W, Abdelly C, Chaïbi W, Smaoui A (2008) Ultrastructure of Aeluropus littoralis leaf salt glands under NaCl stress. Protoplasma 233:195–202. https://doi.org/10.1007/s00709-008-0003-x
Barros CF, Miguens FC (1998) Ultrastructure of the epidermal cells of Beilshmiedia rigida (Mez) Kosterm (Lauraceae). Acta Microsc 7:1–11
Billard B, Field CD (1974) Electrical properties of the salt gland of Aegiceras. Planta 115:285–296. https://doi.org/10.1007/BF00388611
Breckle SW (1995) How do halophytes overcome salinity? In: Khann MA, Ungar IA (Eds.). Biology of salt tolerant plants. Pp 199-213
CABI (2019) Anagallis arvensis. In: In: invasive species compendium. CAB international, Wallingford Https://www.cabi.org/isc accessed 21 august 2019
Cardale S, Field CD (1971) The structure of the salt gland of Aegiceras corniculatum. Planta 99:183–191. https://doi.org/10.1007/BF00386836
Considine JA, Knox RB (1979) Development and histochemistry of the cells, cell walls, and cuticle of the dermal system of fruit of the grape Vitis vinifera L. Protoplasma 99:347–365
Cross BD (1909) Observations on some New Zealand halophytes. Trans Proc New Zeal Inst 42:545–574
Dassanayake M, Larkin JC (2017) Making plants break a sweat: the structure, function, and evolution of plant salt glands. Front Plant Sci 08:1–20. https://doi.org/10.3389/fpls.2017.00406
Fahn A (1979) Secretory tissues in plants. Academic Press, London, p 302
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142. https://doi.org/10.2307/2440500
Field CD, Hinwood EG, Stevenson I (1984) Structural features of the salt gland of Aegiceras. Physiology and management of mangroves
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes*. New Phytol 179:945–963. https://doi.org/10.1111/j.1469-8137.2008.02531.x
Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612. https://doi.org/10.1071/FP09269
Foden W, Potter L (2010) Samolus porosus. The IUCN Red List of Threatened Species e.T185244A8374054.https://doi.org/10.2305/IUCN.UK.2010-3.RLTS.T185244A8374054.en. Accessed 21 August 2019
Freitas MF, Kinoshita LS (2015) Myrsine (Myrsinoideae- Primulaceae) no sudeste e sul do Brasil. Rodriguésia 66:167–189. https://doi.org/10.1590/2175-7860201566109
Freitas MF, Carrijo TT, Luna BN (2017) Sinopse dos gêneros de Primulaceae no Brasil. Rodriguésia 68:129–142. https://doi.org/10.1590/2175-7860201768122
Ghazanfar SA, Altundag E, Yaprak AE, Osborne J, Tug GN, Vural M (2014) Halophytes of Southwest Asia. In: In: Sabkha ecosystems. Springer, Dordrecht
Grigore M-N, Toma C (2017) Anatomical adaptations of halophytes. Springer International Publishing, Cham. https://doi.org/10.1007/978-3-319-66480-4
Grigore M-N, Ivanescu L, Toma C (2014) Halophytes: an integrative anatomical study. Springer International Publishing, Cham
Herth W, Schnepf E (1980) The fluorochrome, calcofluor white, binds oriented to structural polysaccharide fibrils. Protoplasma 105:129–133. https://doi.org/10.1007/BF01279855
Jiang Z, Zhou X, Tao M, Yuan F, Liu L, Wu F, Wu X, Xiang Y, Niu Y, Liu F, Li C, Ye R, Byeon B, Xue Y, Zhao H, Wang HN, Crawford BM, Johnson DM, Hu C, Pei C, Zhou W, Swift GB, Zhang H, Vo-Dinh T, Hu Z, Siedow JN, Pei ZM (2019) Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature. 572:341–346. https://doi.org/10.1038/s41586-019-1449-z
Kamienski F (1880) Vergleichende Anatomie der Primulaceen. Abhand. Naturforsch Ges Halle 14:141–230
Kuster VC, Da Silva Campos L, Possatti L, Schneider SZ (2018) Leaf morphology and anatomy of Jacquinia armillaris Jacq. (Primulaceae) from two coastal restinga environments. Iheringia - Ser Bot 73:240–249. https://doi.org/10.21826/2446-8231201873303
Levering CA, Thomson WW (1971) The ultrastructure of the salt gland of Spartina foliosa. Planta 97:183–196. https://doi.org/10.1007/BF00389200
Luna BN, Defaveri ACA, Sato A, Bizzo HR, Freitas MF, Barros CF (2014) Leaf secretory tissues in Myrsine coriacea and Myrsine venosa (Primulaceae): ontogeny, morphology, and chemical composition of essential oils. Botany 92:757–766. https://doi.org/10.1139/cjb-2014-0044
Luna BN, Freitas MF, Baas P, De Toni KLG, Barros CF (2017) Leaf anatomy of five neotropical genera of Primulaceae. Int J Plant Sci 178:362–377. https://doi.org/10.1086/691213
Luna BN, Freitas MF, Barros CF (2019) Diversity of leaf secretory structures in five Neotropical genera of Primulaceae: ecological aspects and evolutionary significance. Botany 97:35–51. https://doi.org/10.1139/cjb-2018-0114
Meng X, Zhou J, Sui N (2018) Mechanisms of salt tolerance in halophytes: current understanding and recent advances. Open Life Sci 13:149–154. https://doi.org/10.1515/biol-2018-0020
Naidoo Y, Naidoo G (1998) Sporobolus virginicus leaf salt glands: morphology and ultrastructure. S Afr J Bot 64:198–204. https://doi.org/10.1016/S0254-6299(15)30867-X
Naidoo Y, Kasim N, Heneidak S, Nicholas A, Naidoo G (2013) Foliar secretory trichomes of Ocimum obovatum (Lamiaceae): micromorphological structure and histochemistry. Plant Syst Evol 299:873–885. https://doi.org/10.1007/s00606-013-0770-5
Oi T, Miyake H, Taniguchi M (2014) Salt excretion through the cuticle without disintegration of fine structures in the salt glands of Rhodes grass (Chloris gayana Kunth). Flora (Jena) 209:185–190. https://doi.org/10.1016/j.flora.2014.02.004
Öztürk M, Güvensen A, Sakçali S, Görk G (2008) Halophyte plant diversity in the Irano-Turanian phytogeographical region of Turkey. In: Abdelly C, Öztürk M, Ashraf M, Grignon C (Eds.) Biosaline agriculture and high salinity tolerance. Birkhäuser Basel
Reef R, Lovelock CE (2015) Regulation of water balance in mangroves. Ann Bot 115:385–395. https://doi.org/10.1093/aob/mcu174
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212. https://doi.org/10.1083/jcb.17.1.208
Rodrigues TM, Carvalho D, Rodrigues S (2011) The role of the parenchyma sheath and PCD during the development of oil cavities in Pterodon pubescens (Leguminosae-Papilionoideae). C R Biol 334:535–543. https://doi.org/10.1016/j.crvi.2011.04.005
Rozema J, Flowers T (2008) ECOLOGY: crops for a salinized world. Science 322:1478–1480. https://doi.org/10.1126/science.1168572
Rozema J, Riphagen I, Sminia T (1977) A light and electron-microscopical study on the structure and function of the salt gland of Glaux maritima L. New Phytol 79:665–671. https://doi.org/10.1111/j.1469-8137.1977.tb02251.x
Santos J, Al-Azzawi M, Aronson J, Flowers TJ (2016) eHALOPH a database of salt-tolerant plants: helping put halophytes to work. Plant Cell Physiol 57:e10–e10. https://doi.org/10.1093/pcp/pcv155
Scassellati E, Pasqua G, Valletta A, Abbate G (2016) Salt glands of Armeria canescens (Host) Boiss.: morphological and functional aspects. Plant Biosyst 150:1134–1139. https://doi.org/10.1080/11263504.2016.1186126
Shabala S, Bose J, Hedrich R (2014) Salt bladders: do they matter? Trends Plant Sci 19:687–691. https://doi.org/10.1016/j.tplants.2014.09.001
Ståhl B (1992) On the identity of Jacquinia armillaris (Theophrastaceae) and related species. Brittonia 44:54–60. https://doi.org/10.2307/2807442
Stevens PF (2001 Onwards) Angiosperm phylogeny website, version 12, July 2012. http://www.mobot org/MOBOT/research/APweb/. Accessed 13 August 2019
Strasburger E (1924) Handbook of practical botany, 8th edn. George Allen
Thomson WW, Berry WL, Liu LL (1969) Localization and secretion of salt by the salt glands of Tamarix aphylla. PNAS 63:310–317. https://doi.org/10.1073/pnas.63.2.310
von Minden M (1899) Über die Aussonderung wässeriger Lösungen bei den Nicotiana-Arten und Glaux maritima. Die Bedeutung des Epithems bei der Sekretion, part V. Beiträge zur anatomischen und physiologischen Kenntnis Wassersecernierender Organe. Bibl Bot 46:56–76
Water and Rivers Commission (1997) Native vegetation of estuaries and saline waterways in south Western Australia
Wilson H, Mycock D, Weiersbye IM (2017) The salt glands of Tamarix usneoides E. Mey. Ex Bunge (South African Salt Cedar). Int J Phytoremediat 19:587–595. https://doi.org/10.1080/15226514.2016.1244163
Yuan F, Leng B, Wang B (2016) Progress in studying salt secretion from the salt glands in Recretohalophytes: how do plants secrete salt? Front Plant Sci 7:1–12. https://doi.org/10.3389/fpls.2016.00977
Zouhaier B, Abdallah A, Najla T, Wahbi D, Wided C, Aouatef BA, Abderazzak S (2015) Scanning and transmission electron microscopy and X-ray analysisof leaf salt glands of Limoniastrum guyonianum Boiss. Under NaCl salinity. Micron 78:1–9
Acknowledgments
The authors would like to thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the research productivity scholarship awarded to Claudia Franca Barros (process no 310419/2018-2), to Centro Nacional de Biologia Estrutural e Bioimagem (CENABIO) for the microscopical facilities, and to Instituto Estadual do Ambiente (INEA) for the permission to collect the samples evaluated in this study.
Funding
This study was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (153892/2018-8).
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de Luna, B.N., Freitas, M.d., da Silva, K.M.M. et al. Are the glandular trichomes in Jacquinia armillaris (Theophrastoideae—Primulaceae) salt glands?. Protoplasma 257, 863–870 (2020). https://doi.org/10.1007/s00709-019-01472-1
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DOI: https://doi.org/10.1007/s00709-019-01472-1