Abstract
Lycium ruthenicum is a salt-accumulating xerophytic species with excellent adaptability to adverse environments. Previous studies showed that a certain amount of NaCl addition promoted plant growth. To reveal the mechanism underlying the positive effect of Na+ addition on plant growth and investigate the role of moderate NaCl in L. ruthenicum drought resistance, the growth, photosynthesis, and K+ and Na+ transport-related genes were assessed after being subjected to different NaCl (0–400 mM) treatments and osmotic stresses (− 0.5 MPa) in the presence or absence of additional NaCl (50 mM). Compared to the control, 50 mM NaCl strongly boosted the fresh weight, dry weight, relative growth rate, and significantly increased the Na+ concentrations in roots, stems, and leaves; the K+ concentrations in roots and leaves also increased significantly. Furthermore, 50 mM NaCl sharply up-regulated the expression of LrSOS1 in roots and LrNHX and LrVP1 in leaves, while LrHKT1 was down-regulated in roots, this was the reason why a high quantity of Na+ accumulated in leaves. LrAKT1 was up-regulated in roots, and LrSKOR decreased first and then increased in roots, whereas LrSKOR in leaves remained stable and slightly up-regulated, thereby absorbing a large amount of K+ through LrAKT1 and transporting to the leaf through LrSKOR. Moreover, external NaCl apparently alleviated the inhibition of osmotic stress in plant growth, and significantly increased Na+ and K+ concentrations. It is speculated that moderate NaCl treatment could significantly improve the Na+ and K+ concentrations, thus enhancing the osmotic regulation ability of plants, and then improve the photosynthesis and water status of L. ruthenicum.
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Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Overexpression of a vacuolar Na+/H+ antiport confers salt tolerance in Arabidopsis. Science 285:1256–1258
Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmoudi K (2007) Overexpression of wheat Na+/H+ antiporter TNHX1and H+-pyrophosphatase TVP1improve salt-and drought-stress tolerance in Arabidopsis thaliana plants. J Exp Bot 58:301–308
Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246
Dai F, Li A, Rao S, Chen J (2019) Potassium transporter LrKUP8 is essential for K+ preservation in Lycium ruthenicum, a salt-resistant desert shrub. Genes 10(8):600. https://doi.org/10.3390/genes10080600
Davenport RJ, Munoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30:497–507
Debez A, Saadaoui D, Ramani B, Ouerghi Z, Koyro HW, Huchzermeyer B, Abdelly C (2006) Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environ Exp Bot 57:285–295
Duan HR, Ma Q, Zhang JL, Hu J, Bao AK, Wei L, Wang Q, Luan S, Wang SM (2015) The inward-rectifying K+ channel SsAKT1 is a candidate involved in K+ uptake in the halophyte Suaeda salsa under saline condition. Plant Soil 395(1–2):173–187
Epstein E, Bloom A (2005) Mineral nutrition of plants: Principles and perspectives (Sinauer, Sunderland, MA)
Farkhondeh R, Nabizadeh E, Jalilnezhad N (2012) Effect of salinity stress on proline content, membrane stability and water relations in two sugar beet cultivars. Int J Agric Stat Sci 2(5):385–392
Franks PJ, Buckley TN, Shope JC, Mott KA (2001) Guard cell volume and pressure measured concurrently by confocal microscopy and the cell pressure probe. Plant Physiol 125:1577–1584
Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449
Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferrière N, Thibaud J, Sentenac H (1998) Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655
Guo Q, Wang P, Ma Q, Zhang JL, Bao AK, Wang SM (2012) Selective transport capacity for K+ over Na+ is linked to the expression levels of PtSOS1 in halophyte Puccinellia tenuiflora. Func Plant Biol 39:1047–1057
Hasanuzzaman M, Bhuyan M, Nahar K, Hossain MS, Mahmud JA, Hossen MS, Masud AAC, Moumita FM (2018) Potassium: a vital regulator of plant responses and tolerance to abiotic stresses. Agronomy 8(3):1–29. https://doi.org/10.3390/agronomy8030031
Hassine AB, Ghanem ME, Bouzid S, Lutts S (2008) An inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus L. differ in their ability to accumulate proline and glycinebetaine in response to salinity and water stress. J Exp Bot 59:1315–1326
Hu Y, Burucs Z, Tucher SV, Schmidhalter U (2007) Shortterm effects of drought and salinity on mineral nutrient distribution along growing leaves of maize seedlings. Environ Exp Bot 60:268–275
Hu Y, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Plant Nutr Soil Sci 168:541–549
James RA, von Caemmerer S, Condon AG, Zwart AB, Munns R (2008) Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat. Funct Plant Biol 35:111–123
Li JP, Yang XG, Fu H, Zhang BL (2005) The content and distribution characteristics of some osmotic adjusting materials in three species of desert plants in Alashan Desert of Northwest China. Pratacul Sci 22:35–38
Ma Q, Hu J, Xi Z, Yuan H, Kumar T, Luan S, Wang S (2017) ZxAKT1 is essential for K+ uptake and K+/Na+ homeostasis in the succulent xerophyte Zygophyllum xanthoxylum. Plant J 90(1):48–60
Ma Q, Li YX, Yuan HJ, Hu J, Wei L, Bao AK, Zhang JL, Wang SM (2014) ZxSOS1 is essential for long-distance transport and spatial distribution of Na+ and K+ in the xerophyte Zygophyllum xanthoxylum. Plant Soil 374:661–676
Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32:4–13
Maathuis FJM (2014) Sodium in plants: perception signalling and regulation of sodium fluxes. J Exp Bot 65:849–858
Maathuis FJM, Sanders D (2010) Mechanisms of potassium absorption by higher plant roots. Physiol Plantarum 96(1):158–168
Mahi HE, Pérez-Hormaeche J, Luca AD, Villalta I, Espartero J, Gámez-Arjona F, Fernandez JL, Bundo M, Mendoza I, Mieulet D (2019) A critical role of sodium flux via the plasma membrane Na+/H+ exchanger sos1 in the salt tolerance of rice. Plant Physiol 180(2):00324. https://doi.org/10.1104/pp.19.00324
Mahouachi J (2007) Growth and mineral nutrient content of developing fruit on banana plants (Musa acuminata AAA, ‘Grand Nain’) subjected to water stress and recovery. J Pomol Hortic Sci 82:839–844
Maksimovi I, Putnik-Deli M, Gani I, Mari J, Ilin Ž (2010) Growth, ion composition, and stomatal conductance of peas exposed to salinity. Cent Eur J Biol 5(5):682–691
Martínez JP, Lutts S, Schanck A, Bajji M, Kinet JM (2004) Is osmotic adjustment required for water-stress resistance in the Mediterranean shrub Atriplex halimus L.? J Plant Physiol 161:1041–1051
Møller IS, Tester M (2007) Salinity tolerance of Arabidopsis: a good model for cereals? Trends Plant Sci 12:534–540
Moustakas M, Sperdouli I, Kouna T, Antonopoulou CI, Therios I (2011) Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves. Plant Growth Regul 65(2):315–325
Peng Q, Liu H, Shi S, Li M (2014) Lycium ruthenicum polysaccharide attenuates inflammation through inhibiting TLR4/NF-KB signaling pathway. Int J Biol Macromol 67:330–335
Rahnama A, James RA, Poustini K, Munns R (2010) Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Funct Plant Biol 37(3):255–263
Ramanjulu S, Sudhakar C (2000) Proline metabolism during dehydration in two mulberry genotypes withcontrasting drought tolerance. J Plant Physiol 157:81–85
Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytol 190:289–298
Shabala S , Pottosin II (2010) Potassium and potassium-permeable channels in plant salt tolerance. Ion channels and plant stress responses 87−110
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plantar 133:651–669
Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long distance Na+ transport in plants. Plant Cell 14:465–477
Silva EN, Silveira JAG, Rodrigues CRF, Viégas RA (2015) Physiological adjustment to salt stress in Jatropha curcas is associated with accumulation of salt ions transport and selectivity of K+ osmotic adjustment and K+/Na+ homeostasis. Plant Biol 17:1023–1029
Slama I, Ghnaya T, Messedi D, Hessini K, Labidi N, Savoure A, Abdelly C (2007) Effect of sodium chloride on the response of the halophyte species Sesuvium portulacastrum grow in mannitol-induced water stress. J Plant Res 120:291–299
Song X, Wang SM, Jiang Y (2017) Genotypic variations in plant growth and nutritional elements of perennial ryegrass accessions under salinity stress. J Am Soc Hortic Sci 142:476–483
Sunarpi HT, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938
Wang L, Mi Y, Lin H (2011) Effect of salt stress on ion absorption and distribution of two Lycium seedlings. Acta Pratacul Sin 20(4):129–136
Wang SM, Wan CG, Wang YR, Chen H, Zhou ZY, Fu H, Sosebee RE (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China. J Arid Environ 56:525–539
Wang SM, Zhang JL, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145:559–571
Wang WY, Chai WW, Zhao CY, Rowland O, Wang BS, Song X, Liu YQ, Ma Q, Wang SM (2019) Under drought conditions NaCl improves the nutritional status of the xerophyte Zygophyllum xanthoxylum but not of the glycophyte Arabidopsis thaliana. J Plant Nutr Soil Sci 182(5):597–606
Wu GQ, Feng RJ, Liang N, Yuan HJ, Sun WB (2015) Sodium chloride stimulates growth and alleviates sorbitol-induced osmotic stress in sugar beet seedlings. Plant Growth Regul 75:307–316
Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620
Yuan HJ, Ma Q, Wu GQ, Wang P, Hu J, Wang SM (2014) ZxNHX controls Na+ and K+ homeostasis at whole-plant level through feedback regulating the expression of genes involved in their transport in Zygophyllum xanthoxylum. Ann Bot 115(3):495–507
Zhang J, Nguyen H, Blum A (1999) Genetic analysis of osmotic adjustment in crop plants. J Exp Bot 50:291–302
Zhang M, Cao Y, Wang Z, Wang ZQ, Shi J, Liang X, Song W, Chen Q, Lai J, Jiang C (2017) A retrotransposon in an hkt1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize. New Phytol 217(3):1161–1176
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant No. 32060376 and 32060235), the Natural Science Foundation of Gansu Province (Grant No. 20JR5RA093 and 20JR5RA097).
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Supplementary Fig. S1 Effects of different concentration of NaCl treatments on the growth of L. ruthenicum (TIF 25656 KB)
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Supplementary Table S1 Primer sequences used in this study. Real-time quantitative PCR of LrSKOR, LrAKT1, LrHKT1, LrSOS1, LrNHX, LrAPV1, LrLEF1α was performed with the specific primers P1, P2, P3, P4, P5, P6, P7, P8, P9, P10, P11, P12, P13 and P14 (DOCX 18 KB)
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Hu, J., Hu, X., Zhang, H. et al. Moderate NaCl alleviates osmotic stress in Lycium ruthenicum. Plant Growth Regul 96, 25–35 (2022). https://doi.org/10.1007/s10725-021-00754-0
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DOI: https://doi.org/10.1007/s10725-021-00754-0