Research Progress in Salt Gland Secretion and Development in Plants

doi:10.13560/j.cnki.biotech.bull.1985.2023-0581

Abstract

Abstract:

Salt gland is one of the important epidermal structures of recreto-halophytes in resistance to salt stress, which secrete excessive salt ions out of the body to prevent the plant from being damaged by salt stress. As an important structure to achieve high salt resistance in halophytes, salt glands deserve extensive attention and discussion in the fields of stress physiology, development and evolutionary biology. A large number of studies have been reported in the ultrastructure, physiological function, mechanism of salt secretion and developmental pattern of salt glands. In this paper, we reviewed the research progress of salt gland structure, secretion mechanism and salt gland development, summarized the feasible pathways of salt gland secretion and the regulation mode and key genes of salt gland development, proposed relevant views for future research on salt gland secretion and development, and discussed the role of this unique morphological structure of salt gland on plant salt tolerance. We also proposed the theoretical basis and suggestions for improving plant salt tolerance and breeding salt-tolerant plant varieties. The related studies will be beneficial for in-depth analysis of plant salt tolerance adaptation evolution, cultivation of salt resistant crops, and efficient utilization of saline land.

Key words: salt gland, salt gland excretion, salt gland development, salt resistance

MA Qiu-yu, YUAN Fang. Research Progress in Salt Gland Secretion and Development in Plants[J]. Biotechnology Bulletin, 2023, 39(11): 74-85.

Figures/Tables 4

References 95

[1]	Food and Agriculture Organization of the United Nations. The state of the world's land and water resources for food and agriculture: managing systems at risk[M]. Milton Park, Abingdon: Earthscan, 2011.
[2]	Amirhossein H, Adisa A, Nima S. Global predictions of primary soil salinization under changing climate in the 21st century[J]. Nature Communications, 2021, 12(1): 6663. doi: 10.1038/s41467-021-26907-3 pmid: 34795219
[3]	Zhu JK. Regulation of ion homeostasis under salt stress[J]. Curr Opin Plant Biol, 2003, 6(5): 441-445. doi: 10.1016/s1369-5266(03)00085-2 pmid: 12972044
[4]	Flowers TJ, Colmer TD. Plant salt tolerance: adaptations in halophytes[J]. Ann Bot, 2015, 115(3): 327-331. doi: 10.1093/aob/mcu267 URL
[5]	Flowers TJ, Colmer TD. Salinity tolerance in halophytes[J]. New Phytol, 2008, 179(4): 945-963. doi: 10.1111/j.1469-8137.2008.02531.x pmid: 18565144
[6]	Parida AK, Jha B. Salt tolerance mechanisms in mangroves: a review[J]. Trees, 2010, 24(2): 199-217. doi: 10.1007/s00468-010-0417-x URL
[7]	Flowers TJ, Galal HK, Bromham L. Evolution of halophytes: multiple origins of salt tolerance in land plants[J]. Funct Plant Biol, 2010, 37(7): 604. doi: 10.1071/FP09269 URL
[8]	袁芳, 冷冰莹, 王宝山. 植物盐腺泌盐研究进展[J]. 植物生理学报, 2015, 51(10): 1531-1537.
	Yuan F, Leng BY, Wang BS. Research progress in salt secretion of salt glands in plants[J]. Plant Physiol J, 2015, 51(10): 1531-1537.
[9]	Lüttge U. Elimination of salt by recretion: salt glands and gland-supported bladders in recretohalophytes[M]// Halophytes and climate change:adaptive mechanisms and potential uses. UK: CABI, 2019: 223-239.
[10]	Yuan F, Wang BS. Adaptation of recretohalophytes to salinity salt secretion and salt gland development[J]. Handbook of Halophytes: From Molecules to Ecosystems towards Biosaline Agriculture, 2020: 1-21.
[11]	Hokputsa S, Harding SE, Inngjerdingen K, et al. Bioactive polysaccharides from the stems of the Thai medicinal plant Acanthus ebracteatus: their chemical and physical features[J]. Carbohydr Res, 2004, 339(4): 753-762. doi: 10.1016/j.carres.2003.11.022 URL
[12]	Salama FM, El-Naggar SM, Ramadan T. Salt glands of some halophytes in Egypt[J]. Phyton Annales Rei Botanicae, 1999, 39(1): 91-105.
[13]	Mason HL. A flora of the marshes of California[M]. Berkeley: University of California Press, 1957.
[14]	Sayed OH, Hegazy AK. Growth-specific phytomass allocation in Mesembryanthemum nodiflorum as influenced by CAM induction in the field[J]. J Arid Environ, 1994, 27(4): 325-329. doi: 10.1006/jare.1994.1067 URL
[15]	Liu X, Khan M, Tsuji W, et al. The effect of light, temperature and bracteoles on germination of polymorphic seeds of Atriplex centralasiatica Iljin under saline conditions[J]. Seed Science and Technology, 2008, 36(2).
[16]	Gadano AB, Gurni AA, Carballo MA. Argentine folk medicine: genotoxic effects of Chenopodiaceae family[J]. J Ethnopharmacol, 2006, 103(2): 246-251. pmid: 16219440
[17]	Leisner CP, Cousins AB, Offermann S, et al. The effects of salinity on photosynthesis and growth of the single-cell C₄ species Bienertia sinuspersici(Chenopodiaceae)[J]. Photosynth Res, 2010, 106(3): 201-214. doi: 10.1007/s11120-010-9595-z URL
[18]	Doliner LH, Jolliffe PA. Ecological evidence concerning the adaptive significance of the C₄ dicarboxylic acid pathway of photosynthesis[J]. Oecologia, 1979, 38(1): 23-34. doi: 10.1007/BF00347821 pmid: 28309067
[19]	Inamdar JA. Epidermal structure and ontogeny of stomata in some centrospermae[J]. Flora oder Allgemeine botanische Zeitung, 1968, 158(1-2): 159-166.
[20]	Voronkova NM, Burkovskaya EV, Bezdeleva TA, et al. Morphological and biological features of plants related to their adaptation to coastal habitats[J]. Russ J Ecol, 2008, 39: 1-7. doi: 10.1134/S1067413608010013 URL
[21]	Cuadra VP, Cambi V. Morphoanatomical functional traits in xerophytic species of a saline environment[J]. Phyton, 2014, 83: 389-396. doi: 10.32604/phyton.2014.83.389 URL
[22]	Abideen Z, Qasim M, Rizvi RF, et al. Oilseed halophytes: a potential source of biodiesel using saline degraded lands[J]. Biofuels, 2015, 6(5-6): 241-248. doi: 10.1080/17597269.2015.1090812 URL
[23]	Barbour MG, DeJong TM. Response of west coast beach taxa to salt spray, seawater inundation, and soil salinity[J]. Bull Torrey Bot Club, 1977, 104(1): 29-34. doi: 10.2307/2484662 URL
[24]	Pan Y, Wu LJ, Yu ZL. Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice(Glycyrrhiza uralensis Fisch)[J]. Plant Growth Regul, 2006, 49: 157-165. doi: 10.1007/s10725-006-9101-y URL
[25]	Okusanya OT, Fawole T. The possible role of phosphate in the salinity tolerance of Lavatera arborea[J]. J Ecol, 1985, 73(1): 317-322. doi: 10.2307/2259785 URL
[26]	Tattini M, Montagni G, Traversi ML. Gas exchange, water relations and osmotic adjustment in Phillyrea latifolia grown at various salinity concentrations[J]. Tree Physiol, 2002, 22(6): 403-412. doi: 10.1093/treephys/22.6.403 URL
[27]	Mepham RH, Mepham JS. The flora of tidal forests—a rationalization of the use of the term ‘mangrove’[J]. S Afr N J Bot, 1985, 51(2): 77-99.
[28]	Duhazé C, Gouzerh G, Gagneul D, et al. The conversion of spermidine to putrescine and 1, 3-diaminopropane in the roots of Limonium tataricum[J]. Plant Sci, 2002, 163(3): 639-646. doi: 10.1016/S0168-9452(02)00172-3 URL
[29]	Elgorashi EE, Taylor JLS, Maes A, et al. Screening of medicinal plants used in South African traditional medicine for genotoxic effects[J]. Toxicol Lett, 2003, 143(2): 195-207. pmid: 12749823
[30]	Clarke PJ, Kerrigan RA, Westphal CJ. Dispersal potential and early growth in 14 tropical mangroves: do early life history traits correlate with patterns of adult distribution?[J]. J Ecol, 2001, 89(4): 648-659. doi: 10.1046/j.0022-0477.2001.00584.x URL
[31]	Al-Hawija BN, Partzsch M, Hensen I. Effects of temperature, salinity and cold stratification on seed germination in halophytes[J]. Nord J Bot, 2012, 30(5): 627-634. doi: 10.1111/more.2012.30.issue-5 URL
[32]	Al-Sodany YM, Shehata MN, Shaltout KH. Vegetation along an elevation gradient in Al-Jabal Al-Akhdar, Libya[J]. Ecmed, 2003, 29(2): 125-137. doi: 10.3406/ecmed.2003.1547 URL
[33]	Elansary HO, Yessoufou K, Mahmoud EA, et al. In vitro antioxidant and antimicrobial effects of Ceratostigma plumbaginoides[J]. Nat Prod Commun, 2016, 11(10): 1455-1458. pmid: 30549598
[34]	Bustan A, Pasternak D, Pirogova I, et al. Evaluation of saltgrass as a fodder crop for livestock[J]. J Sci Food Agric, 2005, 85(12): 2077-2084. doi: 10.1002/jsfa.v85:12 URL
[35]	Bal AR, Dutt SK. Mechanism of salt tolerance in wild rice(Oryza coarctata Roxb)[J]. Plant Soil, 1986, 92: 399-404. doi: 10.1007/BF02372487 URL
[36]	Atia A, Debez A, Rabhi M, et al. Salt tolerance and potential uses for saline agriculture of halophytes from the Poaceae[M]// Sabkha Ecosystems. Cham: Springer International Publishing, 2019: 223-237.
[37]	Amarasinghe V, Watson L. Variation in salt secretory activity of microhairs in grasses[J]. Funct Plant Biol, 1989, 16(2): 219-229. doi: 10.1071/PP9890219 URL
[38]	Callaway JC, Josselyn MN. The introduction and spread of smooth cordgrass(Spartina alterniflora)in South San Francisco Bay[J]. Estuaries, 1992, 15: 218-226. doi: 10.2307/1352695 URL
[39]	Cuadra VP, Cambi VN. Comparative vegetative anatomy between halophytic Chloridoideae(Poaceae)with forage importance[J]. Phyton, 2010, 79: 69-76. doi: 10.32604/phyton.2010.79.069 URL
[40]	Sathyamoorthy G, Vijay R, Lenin Singaravelu D. Development and characterization of alkali-treated and untreated Dactyloctenium aegyptium fibers based epoxy composites[J]. Mater Today, 2021, 39: 1215-1220.
[41]	Silva Colomer JH, Guevara JC, Marchi A, et al. Native grasses and the nutrition of the breeding cow in the arid plain of Mendoza, Argentina[J]. J Arid Environ, 1991, 20(1): 113-118. doi: 10.1016/S0140-1963(18)30779-1 URL
[42]	Amini V, Zaefarian F, Rezvani M. Interspecific variations in seed germination and seedling emergence of three Setaria species[J]. Braz J Bot, 2015, 38: 539-545. doi: 10.1007/s40415-015-0158-6 URL
[43]	Abbasi SB, Gul B, Khan N, et al. Effect of humic acid on seed germination of sub-tropical halophytes under salt stress[J]. Pak J Bot, 2017, 49(6): 2079-2088.
[44]	Croce P, De Luca A, Mocioni M, et al. Adaptability of warmseason turfgrass species and cultivars in a Mediterranean climate[J]. Acta Hortic, 2004(661): 365-368.
[45]	Czyż H, Kitczak T, Bury M. The characteristics of coastal grassland in West Pomerania[J]. Plant Diversity and Evolution, 2013, 130(3-4): 229-237. doi: 10.1127/1869-6155/2013/0130-0069 URL
[46]	Deng YC, Yang Z, Yu YZ, et al. Inhibitory activity against plant pathogenic fungi of extracts from Myoporum bontioides A. Gray and indentification of active ingredients[J]. Pest Manag Sci, 2008, 64(2): 203-207. doi: 10.1002/ps.v64:2 URL
[47]	Bell HL, Columbus TJ. Proposal for an expanded Distichlis(poac-eae, chloridoideae): support from molecular, morphological, and anatomical characters[J]. Syst Bot, 2008, 33(3): 536-551. doi: 10.1600/036364408785679879 URL
[48]	Wickens GE. Arid lands today and tomorrow. proceedings of an international research and development conference[J]. J Arid Environ, 1989, 16(1): 109-110.
[49]	Dassanayake M, Larkin JC. Making plants break a sweat: the structure, function, and evolution of plant salt glands[J]. Front Plant Sci, 2017, 8: 406. doi: 10.3389/fpls.2017.00406 pmid: 28400779
[50]	薛琼琼, 赵露露, 王云霞, 等. 盐生植物耐盐性研究进展[J]. 中国野生植物资源, 2021, 40(5): 60-65.
	Xue QQ, Zhao LL, Wang YX, et al. Research progress on salt tolerance of halophytes[J]. Chin Wild Plant Resour, 2021, 40(5): 60-65.
[51]	Garg R, Verma M, Agrawal S, et al. Deep transcriptome sequencing of wild halophyte rice, Porteresia coarctata, provides novel insights into the salinity and submergence tolerance factors[J]. DNA Res, 2014, 21(1): 69-84. doi: 10.1093/dnares/dst042 URL
[52]	Semenova GA, Fomina IR, Biel KY. Structural features of the salt glands of the leaf of Distichlis spicata ‘Yensen 4a’(Poaceae)[J]. Protoplasma, 2010, 240(1-4): 75-82. doi: 10.1007/s00709-009-0092-1 pmid: 19997947
[53]	Kuster VC, da Silva LC, Meira RMSA. Anatomical and histochemical evidence of leaf salt glands in Jacquinia armillaris Jacq.(Primulaceae)[J]. Flora, 2020, 262: 151493. doi: 10.1016/j.flora.2019.151493 URL
[54]	韩军丽, 赵可夫. 植物盐腺的结构、功能和泌盐机理的探讨[J]. 山东师大学报: 自然科学版, 2001, 16(2): 194-198.
	Han JL, Zhao KF. The structure, function, and salt-secreted mechanism of salt glands[J]. J Shandong Norm Univ Nat Sci Ed, 2001, 16(2): 194-198.
[55]	Bosabalidis Artemios M. Wall protuberance formation and function in secreting salt glands of Tamarix aphylla L[J]. Acta Bot Croat, 2010, 69(2): 229-235.
[56]	Zhao BQ, Zhou YL, Jiao XM, et al. Bracelet salt glands of the recretohalophyte Limonium bicolor: distribution, morphology, and induction[J]. J Integr Plant Biol, 2023, 65(4): 950-966. doi: 10.1111/jipb.v65.4 URL
[57]	Deng YQ, Feng ZT, Yuan F, et al. Identification and functional analysis of the autofluorescent substance in Limonium bicolor salt glands[J]. Plant Physiol Biochem, 2015, 97: 20-27. doi: 10.1016/j.plaphy.2015.09.007 URL
[58]	Yuan F, Chen M, Leng BY, et al. An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion[J]. S Afr J Bot, 2013, 88: 110-117. doi: 10.1016/j.sajb.2013.06.007 URL
[59]	Balsamo RA, Thomson WW. Ultrastructural features associated with secretion in the salt glands of Frankenia grandifolia(Frankeniaceae)and Avicennia germinans(Avicenniaceae)[J]. Am J Bot, 1993, 80(11): 1276-1283. doi: 10.1002/ajb2.1993.80.issue-11 URL
[60]	Ding F, Yang JC, Yuan F, et al. Progress in mechanism of salt excretion in recretohalopytes[J]. Front Biol, 2010, 5: 164-170. doi: 10.1007/s11515-010-0032-7 URL
[61]	Overall RL, Blackman LM. A model of the macromolecular structure of plasmodesmata[J]. Trends Plant Sci, 1996, 1(9): 307-311. doi: 10.1016/S1360-1385(96)88177-0 URL
[62]	Yuan F, Lyu MJA, Leng BY, et al. Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation[J]. Plant Cell Environ, 2015, 38(8): 1637-1657. doi: 10.1111/pce.2015.38.issue-8 URL
[63]	Flowers TJ, Flowers SA, Hajibagheri MA, et al. Salt tolerance in the halophytic wild rice, Porteresia coarctata Tateoka[J]. New Phytol, 1990, 114(4): 675-684. doi: 10.1111/nph.1990.114.issue-4 URL
[64]	Storey R, Thomson WW. An X-ray microanalysis study of the salt glands and intracellular calcium crystals of Tamarix[J]. Ann Bot, 1994, 73(3): 307-313. doi: 10.1006/anbo.1994.1036 URL
[65]	Sobrado MA, Greaves ED. Leaf secretion composition of the mangrove species Avicennia germinans(L.) in relation to salinity: a case study by using total-reflection X-ray fluorescence analysis[J]. Plant Sci, 2000, 159(1): 1-5. pmid: 11011087
[66]	Han MX, Yang H, Yu G, et al. Application of Non-invasive Micro-test Technology(NMT)in environmental fields: a comprehensive review[J]. Ecotoxicol Environ Saf, 2022, 240: 113706. doi: 10.1016/j.ecoenv.2022.113706 URL
[67]	Feng ZT, Deng YQ, Zhang SC, et al. 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[J]. Plant Sci, 2015, 238: 286-296. doi: 10.1016/j.plantsci.2015.06.021 URL
[68]	Arisz WH, Camphuis IJ, Heikens H, et al. The secretion of the salt glands of Limonium latifolium ktze[J]. Acta Bot Neerl, 1955, 4(3): 322-338. doi: 10.1111/plb.1955.4.issue-3 URL
[69]	Levering CA, Thomson WW. The ultrastructure of the salt gland of Spartina foliosa[J]. Planta, 1971, 97(3): 183-196. doi: 10.1007/BF00389200 pmid: 24493239
[70]	Kobayashi H, Masaoka Y, Takahashi Y, et al. Ability of salt glands in Rhodes grass(Chloris gayana Kunth)to secrete Na⁺ and K⁺[J]. Soil Sci Plant Nutr, 2007, 53(6): 764-771. doi: 10.1111/j.1747-0765.2007.00192.x URL
[71]	Ma HY, Tian CY, Feng G, et al. Ability of multicellular salt glands in Tamarix species to secrete Na⁺and K⁺ selectively[J]. Sci China Life Sci, 2011, 54(3): 282-289. doi: 10.1007/s11427-011-4145-2 URL
[72]	Shimony C, Fahn A. Light- and electron-microscopical studies on the structure of salt glands of Tamarix aphylla L[J]. J Linn Soc Lond Bot, 1968, 60(383): 283-288. doi: 10.1111/boj.1968.60.issue-383 URL
[73]	Thomson WW, Berry WL, Liu LL. Localization and secretion of salt by the salt glands of tamarix aphylla[J]. Proc Natl Acad Sci U S A, 1969, 63(2): 310-317. doi: 10.1073/pnas.63.2.310 URL
[74]	Lu CX, Feng ZT, Yuan F, et al. The SNARE protein LbSYP61 participates in salt secretion in Limonium bicolor[J]. Environ Exp Bot, 2020, 176: 104076. doi: 10.1016/j.envexpbot.2020.104076 URL
[75]	Zhang WD, Wang P, Bao Z, et al. SOS1, HKT1;5, and NHX1 synergistically modulate Na⁺ homeostasis in the halophytic grass Puccinellia tenuiflora[J]. Front Plant Sci, 2017, 8: 576.
[76]	Ma Q, Li YX, Yuan HJ, et al. ZxSOS1 is essential for long-distance transport and spatial distribution of Na⁺ and K⁺ in the xerophyte Zygophyllum xanthoxylum[J]. Plant Soil, 2014, 374: 661-676. doi: 10.1007/s11104-013-1891-x URL
[77]	Colmenero-Flores JM, Martínez G, Gamba G, et al. Identification and functional characterization of cation-chloride cotransporters in plants[J]. Plant J, 2007, 50(2): 278-292. pmid: 17355435
[78]	杨剑超, 丁烽, 吴蕊蕊, 等. 不同阴离子对二色补血草盐腺Na⁺分泌速率的影响[J]. 植物生理学报, 2012, 48(4): 397-402.
	Yang JC, Ding F, Wu RR, et al. Effects of different anions on Na⁺ secretion rate of salt glands in the leaves of Limonium bicolor[J]. Plant Physiol J, 2012, 48(4): 397-402.
[79]	Sanadhya P, Agarwal P, Khedia J, et al. A low-affinity K⁺ transporter AlHKT2;1 from recretohalophyte Aeluropus lagopoides confers salt tolerance in yeast[J]. Mol Biotechnol, 2015, 57: 489-498. doi: 10.1007/s12033-015-9842-9 pmid: 25604033
[80]	Balsamo RA, Adams ME, Thomson WW. Electrophysiology of the salt glands of Avicennia germinans[J]. Int J Plant Sci, 1995, 156(5): 658-667. doi: 10.1086/297288 URL
[81]	Dschida WJ, Platt-Aloia KA, Thomson WW. Epidermal peels of Avicennia germinans(L.) stearn: a useful system to study the function of salt glands[J]. Ann Bot, 1992, 70(6): 501-509. doi: 10.1093/oxfordjournals.aob.a088510 URL
[82]	丁烽. 二色补血草叶片盐腺泌盐机理的研究[D]. 济南: 山东师范大学, 2010.
	Ding F. The salt-secretion mechanism of salt glands in the leaves of Limonium[D]. Jinan: Shandong Normal University, 2010.
[83]	Debez A, Saadaoui D, Ramani B, et al. Leaf H⁺-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity[J]. Environ Exp Bot, 2006, 57(3): 285-295. doi: 10.1016/j.envexpbot.2005.06.009 URL
[84]	Chen J, Xiao Q, Wu FH, et al. Nitric oxide enhances salt secretion and Na⁺sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H⁺ -ATPase and Na⁺ /H⁺ antiporter under high salinity[J]. Tree Physiol, 2010, 30(12): 1570-1585. doi: 10.1093/treephys/tpq086 URL
[85]	Shi HZ, Zhu JK. Regulation of expression of the vacuolar Na⁺/H⁺ antiporter gene AtNHX1 by salt stress and abscisic acid[J]. Plant Mol Biol, 2002, 50(3): 543-550. doi: 10.1023/A:1019859319617 URL
[86]	Wiehe W, Breckle SW. Die ontogenese der Salzdrüsen von Limonium(Plumbaginaceae); The ontogenesis of the salt glands of Limonium(Plumbaginaceae)[J]. Botanica Acta, 1990, 103(1): 107-110. doi: 10.1111/plb.1990.103.issue-1 URL
[87]	Leng BY, Yuan F, Dong XX, et al. Distribution pattern and salt excretion rate of salt glands in two recretohalophyte species of Limonium(Plumbaginaceae)[J]. S Afr N J Bot, 2018, 115: 74-80.
[88]	Yuan F, Wang X, Zhao BQ, et al. The genome of the recretohalophyte Limonium bicolor provides insights into salt gland development and salinity adaptation during terrestrial evolution[J]. Mol Plant, 2022, 15(6): 1024-1044. doi: 10.1016/j.molp.2022.04.011 URL
[89]	Breckle SW. Salinity tolerance of different halophyte types[M]// Genetic Aspects of Plant Mineral Nutrition. Dordrecht: Springer Netherlands, 1990: 167-175.
[90]	Zhao MZ, Morohashi K, Hatlestad G, et al. The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci[J]. Development, 2008, 135(11): 1991-1999. doi: 10.1242/dev.016873 pmid: 18434419
[91]	Jiao XM, Zhao BQ, Wang BS, et al. An uncharacterized gene Lb1G04794 from Limonium bicolor promotes salt tolerance and trichome development in Arabidopsis[J]. Front Plant Sci, 2022, 13: 1079534. doi: 10.3389/fpls.2022.1079534 URL
[92]	Wang X, Zhou YL, Xu YY, et al. A novel gene LbHLH from the halophyte Limonium bicolor enhances salt tolerance via reducing root hair development and enhancing osmotic resistance[J]. BMC Plant Biol, 2021, 21(1): 284. doi: 10.1186/s12870-021-03094-3 pmid: 34157974
[93]	Leng BY, Wang X, Yuan F, et al. Heterologous expression of the Limonium bicolor MYB transcription factor LbTRY in Arabidopsis thaliana increases salt sensitivity by modifying root hair development and osmotic homeostasis[J]. Plant Sci, 2021, 302: 110704. doi: 10.1016/j.plantsci.2020.110704 URL
[94]	Zou H, Leng BY, Gao YR, et al. The MYB transcription factor LbCPC of Limonium bicolor negatively regulates salt gland development and salt tolerance[J]. Environ Exp Bot, 2023, 209: 105310. doi: 10.1016/j.envexpbot.2023.105310 URL
[95]	Xu YY, Jiao XM, Wang X, et al. Importin-β from the recretohalophyte Limonium bicolor enhances salt tolerance in Arabidopsis thaliana by reducing root hair development and abscisic acid sensitivity[J]. Front Plant Sci, 2021, 11: 582459. doi: 10.3389/fpls.2020.582459 URL

Family	Genus	Species	Reference
Acanthaceae	Acanthus	A. ebracteatus, A. ilicifolius	[11]
Acanthaceae	Avicennia	A. germinans, A. marina, A. officinalis, A. schaueriana, A. bicolor	[12]
Aizoaceae	Sesuvium	S. sesuvioides, S. portulacastrum	[13]
Aizoaceae	Mesembryanthemum	M. nodiflorum, M. crystallinum	[14]
Amaranthaceae	Atriplex	A. farinosa, A. centralasiatica, A. confertifolia, A. hortensis, A. hymenelytra, A. laciniata, A. micrantha, A. oestophora, A. patens, A. portulacoides, A. rosea, A. prostrata, A. prostrata, A. tatarica, A. verrucifera, A. littoralis, A. nummularia, A. cristata, A. canescens, A. halimus, A. semibaccata, A. vesicaria, A. spongiosa, A. amnicola, A. lindleyi, A. turcomanica	[15]
Amaranthaceae	Chenopodium	C. album	[16]
Amaranthaceae	Bienertia	B. sinuspersici	[17]
Amaranthaceae	Oxybasis	O. glauca	[18]
Amaranthaceae	Chenopodiastrum	C. murale	[19]
Apiaceae	Glehnia	G. littoralGis	[20]
Asteraceae	Pseudobaccharis	P. spartioides	[21]
Convolvulaceae	Cressa	C. cretica	[22]
Convolvulaceae	Calystegia	C. soldanella	[23]
Fabaceae	Glycyrrhiza	G. uralensis	[24]
Frankeniaceae	Frankenia	F. juniperoides, F. pauciflora, F. corymbosa, F. salina, F. hirsuta, F. laevis, F. pulverulenta, F. thymifolia	[21]
Malvaceae	Malva	M. arborea	[25]
Oleaceae	Phillyrea	P. latifolia	[26]
Plumbaginaceae	Limonium	L. otolepis, L. suffruticosum, L. reniforme, L. santapolense, L. girardianum, L. platyphyllum, L. bellidifolium, L. binervosum, L. nudum, L. aureum, L. axillare, L. iranicum, L. lobatum, L. oleifolium, L. virgatum, L. pectinatum, L. perezii, L. sinense, L. sinuatum, L. stocksii, L. franchetii, L. bicolor, L. caspium, L. pruinosum, L. gmelinii, L. vulgare, L. brasiliense, L. californicum, L. narbonense, L. delicatulum, L. ovalifolium, L. ovalifolium	[27]
Plumbaginaceae	Goniolimon	G. tataricum	[28]
Plumbaginaceae	Plumbago	P. auriculata	[29]
Plumbaginaceae	Aegialitis	A. annulata, A. rotundifolia	[30]
Plumbaginaceae	Armeria	A. maritima	[31]
Plumbaginaceae	Limoniastrum	L. monopetalum, L. guyonianum	[32]
Plumbaginaceae	Ceratostigma	C. plumbaginoides	[33]
Poaceae	Distichlis	D. humilis, D. spicata	[34]
Poaceae	Oryza	O. coarctata	[35]
Poaceae	Odyssea	O. paucinervis	[36]
Poaceae	Spinifex	S. hirsutus	[37]
Poaceae	Sporobolus	S. foliosus, S. montevidensis, S. xtownsendii, S. helvolus, S. virginicus, S. airoides, S. spicatus, S. michauxianus, S. ioclados, S. alterniflorus, S. anglicus, S. pungens, S. maritimus	[38]
Poaceae	Leptochloa	L. crinita	[39]
Poaceae	Zoysia	Z. macrantha, Z. matrella, Z. macrostachya, Z. japonica, Z. matrella	[37]
Poaceae	Chloris	C. gayana	[37]
Poaceae	Cynodon	C. dactylon	[37]
Poaceae	Dactyloctenium	D. aegyptium	[40]
Poaceae	Diplachne	D. fusca	[37]
Poaceae	Eleusine	E. indica	[37]
Poaceae	Panicum	P. virgatum	[37]
Poaceae	Pappophorum	P. philippianum	[41]
Poaceae	Setaria	S. viridis	[42]
Poaceae	Aeluropus	A. lagopoides, A. littoralis	[43]
22Poaceae	Imperata	I. cylindrica	[37]
Poaceae	Cenchrus	C. clandestinum	[37]
Poaceae	Bouteloua	B. dactyloides	[44]
Primulaceae	Lysimachia	L. maritima	[45]
Primulaceae	Aegiceras	A. floridum, A. corniculatum	[11]
Scrophulariaceae	Myoporum	M. bontioides	[46]
Tamaricaceae	Reaumuria	R. alternifolia, R. hirtella, R. trigyna	[47]
Tamaricaceae	Tamarix	T. amplexicaulis, T. arborea, T. karelini, T. gansuensisi, T. smyrnensis, T. passerinoides, T. laxa, T. hispida, T. elongata, T. austromongolica, T. arceuthoides, T. nilotica, T. africana, T. usneoides, T. chinensis, T. ramosissima, T. aphylla, T. hohenackeri, T. gallica	[48]
Verbenaceae	Phyla	P. nodiflora	[48]

Family	Genus	Species	Reference
Acanthaceae	Acanthus	A. ebracteatus, A. ilicifolius	[11]
Acanthaceae	Avicennia	A. germinans, A. marina, A. officinalis, A. schaueriana, A. bicolor	[12]
Aizoaceae	Sesuvium	S. sesuvioides, S. portulacastrum	[13]
Aizoaceae	Mesembryanthemum	M. nodiflorum, M. crystallinum	[14]
Amaranthaceae	Atriplex	A. farinosa, A. centralasiatica, A. confertifolia, A. hortensis, A. hymenelytra, A. laciniata, A. micrantha, A. oestophora, A. patens, A. portulacoides, A. rosea, A. prostrata, A. prostrata, A. tatarica, A. verrucifera, A. littoralis, A. nummularia, A. cristata, A. canescens, A. halimus, A. semibaccata, A. vesicaria, A. spongiosa, A. amnicola, A. lindleyi, A. turcomanica	[15]
Amaranthaceae	Chenopodium	C. album	[16]
Amaranthaceae	Bienertia	B. sinuspersici	[17]
Amaranthaceae	Oxybasis	O. glauca	[18]
Amaranthaceae	Chenopodiastrum	C. murale	[19]
Apiaceae	Glehnia	G. littoralGis	[20]
Asteraceae	Pseudobaccharis	P. spartioides	[21]
Convolvulaceae	Cressa	C. cretica	[22]
Convolvulaceae	Calystegia	C. soldanella	[23]
Fabaceae	Glycyrrhiza	G. uralensis	[24]
Frankeniaceae	Frankenia	F. juniperoides, F. pauciflora, F. corymbosa, F. salina, F. hirsuta, F. laevis, F. pulverulenta, F. thymifolia	[21]
Malvaceae	Malva	M. arborea	[25]
Oleaceae	Phillyrea	P. latifolia	[26]
Plumbaginaceae	Limonium	L. otolepis, L. suffruticosum, L. reniforme, L. santapolense, L. girardianum, L. platyphyllum, L. bellidifolium, L. binervosum, L. nudum, L. aureum, L. axillare, L. iranicum, L. lobatum, L. oleifolium, L. virgatum, L. pectinatum, L. perezii, L. sinense, L. sinuatum, L. stocksii, L. franchetii, L. bicolor, L. caspium, L. pruinosum, L. gmelinii, L. vulgare, L. brasiliense, L. californicum, L. narbonense, L. delicatulum, L. ovalifolium, L. ovalifolium	[27]
Plumbaginaceae	Goniolimon	G. tataricum	[28]
Plumbaginaceae	Plumbago	P. auriculata	[29]
Plumbaginaceae	Aegialitis	A. annulata, A. rotundifolia	[30]
Plumbaginaceae	Armeria	A. maritima	[31]
Plumbaginaceae	Limoniastrum	L. monopetalum, L. guyonianum	[32]
Plumbaginaceae	Ceratostigma	C. plumbaginoides	[33]
Poaceae	Distichlis	D. humilis, D. spicata	[34]
Poaceae	Oryza	O. coarctata	[35]
Poaceae	Odyssea	O. paucinervis	[36]
Poaceae	Spinifex	S. hirsutus	[37]
Poaceae	Sporobolus	S. foliosus, S. montevidensis, S. xtownsendii, S. helvolus, S. virginicus, S. airoides, S. spicatus, S. michauxianus, S. ioclados, S. alterniflorus, S. anglicus, S. pungens, S. maritimus	[38]
Poaceae	Leptochloa	L. crinita	[39]
Poaceae	Zoysia	Z. macrantha, Z. matrella, Z. macrostachya, Z. japonica, Z. matrella	[37]
Poaceae	Chloris	C. gayana	[37]
Poaceae	Cynodon	C. dactylon	[37]
Poaceae	Dactyloctenium	D. aegyptium	[40]
Poaceae	Diplachne	D. fusca	[37]
Poaceae	Eleusine	E. indica	[37]
Poaceae	Panicum	P. virgatum	[37]
Poaceae	Pappophorum	P. philippianum	[41]
Poaceae	Setaria	S. viridis	[42]
Poaceae	Aeluropus	A. lagopoides, A. littoralis	[43]
22Poaceae	Imperata	I. cylindrica	[37]
Poaceae	Cenchrus	C. clandestinum	[37]
Poaceae	Bouteloua	B. dactyloides	[44]
Primulaceae	Lysimachia	L. maritima	[45]
Primulaceae	Aegiceras	A. floridum, A. corniculatum	[11]
Scrophulariaceae	Myoporum	M. bontioides	[46]
Tamaricaceae	Reaumuria	R. alternifolia, R. hirtella, R. trigyna	[47]
Tamaricaceae	Tamarix	T. amplexicaulis, T. arborea, T. karelini, T. gansuensisi, T. smyrnensis, T. passerinoides, T. laxa, T. hispida, T. elongata, T. austromongolica, T. arceuthoides, T. nilotica, T. africana, T. usneoides, T. chinensis, T. ramosissima, T. aphylla, T. hohenackeri, T. gallica	[48]
Verbenaceae	Phyla	P. nodiflora	[48]

基因 Gene	蛋白质 Protein	功能 Function	参考文献 Reference
NHX1	Na⁺/H⁺逆向转运蛋白	将Na⁺泵出细胞外或储存在液泡	[75]
NHX7	Na⁺/H⁺逆向转运蛋白	将Na⁺泵出细胞外或储存在液泡	[76]
AtCCC、NKCC	Na⁺:K⁺:Cl^-共转运体	参与Cl^-的长距离运输	[77-78]
AlHKT2;1	高亲和性钾转运蛋白	将Na⁺泵入细胞	[79]

基因 Gene	蛋白质 Protein	功能 Function	参考文献 Reference
NHX1	Na⁺/H⁺逆向转运蛋白	将Na⁺泵出细胞外或储存在液泡	[75]
NHX7	Na⁺/H⁺逆向转运蛋白	将Na⁺泵出细胞外或储存在液泡	[76]
AtCCC、NKCC	Na⁺:K⁺:Cl^-共转运体	参与Cl^-的长距离运输	[77-78]
AlHKT2;1	高亲和性钾转运蛋白	将Na⁺泵入细胞	[79]

转录因子 Transcription factor	基因 Gene	功能 Function	参考文献 Reference
bHLH	ENHANCER OF GLABRA3（EGL3）, LbHLH	盐腺发育的负调节因子	[88,92]
MYB	TRIPTYCHON（TRY）	盐腺发育的负调节因子	[88,93]
MYB	CAPRICE（CPC）	盐腺发育的负调节因子	[88,94]
WD40 repeat-like superfamily	TRANSPARENT TESTA GLABRA1（TTG1）	盐腺发育的负调节因子	[88]
ARM repeat superfamily	SENSITIVE TO ABA AND DROUGHT2（SAD2）	盐腺发育的正调节因子	[88,95]
NAC	LbNAC4	盐腺发育的正调节因子	[56]