Abstract
Aims
Na+/H+ antiporter (NHX1) was reported to be induced by NaCl in plants and NaCl can alleviate the toxic effect in plants caused by cadmium (Cd). However, it is unknown whether the NHX1 gene is involved in Cd adaptation in plants. This study aimed to explore the relationship between Cd resistance and NHX1 in plants.
Methods
SseNHX1 gene obtained by shuffling using SsNHX1 from Suaeda salsa and SeNHX1 from Salicornia europaea as sequence templates in our previous work, conferred higher salt tolerance to yeast than SsNHX1 and SeNHX1. The overexpression of SsNHX1, SeNHX1, or SseNHX1 genes in tobacco was performed to explore the relationship between Cd resistance and NHX1 gene expression in plants. The NHX1 inhibitor amiloride was also used to assess the relationship between Cd resistance and NHX1 in plants.
Results
Under Cd stress treatment, transgenic tobacco exhibited better growth status, increased chlorophyll content, improved photosynthesis capacity and enhanced content of Na+ and K+ compared to wildtype plants. Moreover, transgenic tobacco showed less ROS accumulation, reduced MDA production, and decreased Cd2+ accumulation compared to WT plants. More importantly, transgenic tobaccos overexpressing SseNHX1 gene showed a greater resistance to Cd stress and less Cd accumulation than the transgenic tobaccos overexpressing SsNHX1 or SeNHX1 genes.
Conclusions
Cd resistance and Cd accumulation in transgenic tobacco plants was closely correlated with the expression of NHX1 gene.
Similar content being viewed by others
References
Abbasi GH, Akhtar J, Anwar-ul-Haq M, Malik W, Ali S, Chen Z, Zhang G (2015) Morpho-physiological and micrographic characterization of maize hybrids under NaCl and Cd stress. Plant Growth Regul 75:115–122. https://doi.org/10.1007/s10725-014-9936-6
Bahmani R, Modareszadeh M, Kim D, Hwang S (2019) Overexpression of tobacco UBQ2 increases Cd tolerance by decreasing Cd accumulation and oxidative stress in tobacco and Arabidopsis. Environ Exp Bot 166:103805. https://doi.org/10.1016/j.envexpbot.2019.103805
Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active ptassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant cell 24:1127. https://doi.org/10.1105/tpc.111.095273
Bassil E, Blumwald E (2014) The ins and outs of intracellular ion homeostasis: NHX-type cation/H+ transporters. Curr Opin Plant Biol 22:1–6. https://doi.org/10.1016/j.pbi.2014.08.002
Bassil E, Tajima H, Liang YC, Ohto M-a, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011) The Arabidopsis Na+/H+ Antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant cell 23:3482. https://doi.org/10.1105/tpc.111.089581
Bi Y, Chen W, Zhang W, Zhou Q, Yun L, Xing D (2009) Production of reactive oxygen species, impairment of photosynthetic function and dynamic changes in mitochondria are early events in cadmium-induced cell death in Arabidopsis thaliana. Biol Cell 101:629–643. https://doi.org/10.1042/BC20090015
Blumwald E, Poole RJ (1985) Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiol 78:163. https://doi.org/10.1104/pp.78.1.163
Bora MS, Gogoi N, Sarma KP (2020) Tolerance mechanism of cadmium in Ceratopteris pteridoides: Translocation and subcellular distribution. Ecotoxicol Environ Saf 197:110599. https://doi.org/10.1016/j.ecoenv.2020.110599
Burzyński M, Kolano E (2003) In vivo and in vitro effects of copper and cadmium on the plasma membrane H+-ATPase from cucumber (Cucumis sativus L.) and maize (Zea mays L.) roots. Acta Physiol Plant 25:39–45. https://doi.org/10.1007/s11738-003-0034-z
Cai LM, Wang QS, Wen HH, Luo J, Wang S (2019) Heavy metals in agricultural soils from a typical township in Guangdong Province, China: Occurrences and spatial distribution. Ecotoxicol Environ Saf 168:184–191. https://doi.org/10.1016/j.ecoenv.2018.10.092
Cao F, Chen F, Sun H, Zhang G, Chen Z, Wu F (2014) Genome-wide transcriptome and functional analysis of two contrasting genotypes reveals key genes for cadmium tolerance in barley. BMC Genom 15:611. https://doi.org/10.1186/1471-2164-15-611
Carius AB, Rogne P, Duchoslav M, Wolf-Watz M, Samuelsson G, Shutova T (2019) Dynamic pH-induced conformational changes of the PsbO protein in the fluctuating acidity of the thylakoid lumen. Physiol Plant 166:288–299. https://doi.org/10.1111/ppl.12948
Chen X, Bao H, Guo J, Jia W, Tai F, Nie L, Jiang P, Feng J, Lv S, Li Y (2014) Na+/H+ exchanger 1 participates in tobacco disease defence against Phytophthora parasitica var. nicotianae by affecting vacuolar pH and priming the antioxidative system. J Exp Bot 65:6107–6122. https://doi.org/10.1093/jxb/eru351
Chrysargyris A, Papakyriakou E, Petropoulos SA, Tzortzakis N (2019) The combined and single effect of salinity and copper stress on growth and quality of Mentha spicata plants. J Hazard Mater 368:584–593. https://doi.org/10.1016/j.jhazmat.2019.01.058
Chrysargyris A, Solomou M, Petropoulos SA, Tzortzakis N (2019) Physiological and biochemical attributes of Mentha spicata when subjected to saline conditions and cation foliar application. J Plant Physiol 232:27–38. https://doi.org/10.1016/j.jplph.2018.10.024
Cong M, Lv J, Liu X, Zhao J, Wu H (2013) Gene expression responses in Suaeda salsa after cadmium exposure. SpringerPlus 2:232. https://doi.org/10.1186/2193-1801-2-232
Darley CP, Van Wuytswinkel OCM, Van Der Woude K, Mager WH, De Boer AH (2000) Arabidopsis thaliana and Saccharomyces cerevisiae NHX1 genes encode amiloride sensitive electroneutral Na+/H+ exchangers. Biochem J 351:241–249
D’Onofrio C, Lindberg S (2009) Sodium induces simultaneous changes in cytosolic calcium and pH in salt-tolerant quince protoplasts. J Plant Physiol 166:1755–1763. https://doi.org/10.1016/j.jplph.2009.05.006
Dragwidge JM, Scholl S, Schumacher K, Gendall AR (2019) NHX-type Na+(K+)/H+ antiporters are required for TGN/EE trafficking and endosomal ion homeostasis in Arabidopsis thaliana. J Cell Sci 132:jcs226472. https://doi.org/10.1242/jcs.226472
Feng X, Liu W, Zeng F, Chen Z, Zhang G, Wu F (2016) K+ uptake, H+-ATPase pumping activity and Ca2+ efflux mechanism are involved in drought tolerance of barley. Environ Exp Bot 129:57–66. https://doi.org/10.1016/j.envexpbot.2015.11.006
Gajewska E, Skłodowska M (2007) Effect of nickel on ROS content and antioxidative enzyme activitiesin wheat leaves. Biometals 20:27–36. https://doi.org/10.1007/s10534-006-9011-5
Gilliham M, Conn S (2010) Comparative physiology of elemental distributions in plants. Ann Bot 105:1081–1102. https://doi.org/10.1093/aob/mcq027
Gorinova N, Nedkovska M, Todorovska E, Simova-Stoilova L, Stoyanova Z, Georgieva K, Demirevska-Kepova K, Atanassov A, Herzig R (2007) Improved phytoaccumulation of cadmium by genetically modified tobacco plants (Nicotiana tabacum L.). Physiological and biochemical response of the transformants to cadmium toxicity. Environ Pollut 145:161–170. https://doi.org/10.1016/j.envpol.2006.03.025
Gouiaa S, Khoudi H (2019) Expression of V-PPase proton pump, singly or in combination with a NHX1 transporter, in transgenic tobacco improves copper tolerance and accumulation. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-019-06852-x
Goussi R, Manaa A, Derbali W, Ghnaya T, Abdelly C, Barbato R (2018) Combined effects of NaCl and Cd2+ stress on the photosynthetic apparatus of Thellungiella salsuginea. Biochim Biophys Acta 1859:1274–1287. https://doi.org/10.1016/j.bbabio.2018.10.001
Guo Q, Meng L, Zhang Y, Mao P, Tian X, Li S, Zhang L (2017) Antioxidative systems, metal ion homeostasis and cadmium distribution in Iris lactea exposed to cadmium stress. Ecotoxicol Environ Saf 139:50–55. https://doi.org/10.1016/j.ecoenv.2016.12.013
Han RM, Lefèvre I, Albacete A, Pérez Alfocea F, Barba Espín G, Díaz Vivancos P, Quinet M, Ruan C-J, Hernández JA, Cantero Navarro E, Lutts S (2013) Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte Kosteletzkya virginica under saline conditions. Physiol Plant 147:352–368. https://doi.org/10.1111/j.1399-3054.2012.01667.x
Hideg É, Schreiber U (2007) Parallel assessment of ROS formation and photosynthesis in leaves by fluorescence imaging. Photosynth Res 92:103–108. https://doi.org/10.1007/s11120-007-9146-4
Horsch R, Fry J, Wallroth NLH, Eichholtz M, Rogers DS, et al (1985) A simple and general method for transferring genes into plants. Science (New York, NY) 227:1229–1231. https://doi.org/10.1126/science.227.4691.1229
Huang Y, Guan C, Liu Y, Chen B, Yuan S, Cui X, Zhang Y, Yang F (2017) Enhanced growth performance and salinity tolerance in transgenic switchgrass via overexpressing vacuolar Na+(K+)/H+ antiporter gene (PvNHX1). Front Plant Sci 8:458
Iannone MF, Groppa MD, Benavides MP (2015) Cadmium induces different biochemical responses in wild type and catalase-deficient tobacco plants. Environ Exp Bot 109:201–211. https://doi.org/10.1016/j.envexpbot.2014.07.008
Ishak NK, Sulaiman Z, Tennakoon KU (2015) Comparative study on growth performance of transgenic (over-expressed OsNHX1) and wild-type nipponbare under different salinity regimes. Rice Sci 22:275–282. https://doi.org/10.1016/j.rsci.2015.06.002
Janicka-Russak M, Kabała K, Burzyński M (2012) Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. J Exp Bot 63:4133–4142. https://doi.org/10.1093/jxb/ers097
Joshi R, Mangu VR, Bedre R, Sanchez L, Pilcher W, Zandkarimi H, Baisakh N (2015) Salt adaptation mechanisms of halophytes: improvement of salt tolerance in crop plants. In: Pandey GK (eds) Elucidation of Abiotic Stress Signaling in Plants: Functional Genomics Perspectives. Springer, New York
Kanai M, Higuchi K, Hagihara T, Konishi T, Ishii T, Fujita N, Nakamura Y, Maeda Y, Yoshiba M, Tadano T (2007) Common reed produces starch granules at the shoot base in response to salt stress. New Phytol 176:572–580. https://doi.org/10.1111/j.1469-8137.2007.02188.x
Khoudi H, Maatar Y, Gouiaa S, Masmoudi K (2012) Transgenic tobacco plants expressing ectopically wheat Hâ+º-pyrophosphatase (Hâ+º-PPase) gene TaVP1 show enhanced accumulation and tolerance to cadmium. J Plant Physiol 169:98–103. https://doi.org/10.1016/j.jplph.2011.07.016
Kicińska A (2019) Environmental risk related to presence and mobility of As, Cd and Tl in soils in the vicinity of a metallurgical plant – Long-term observations. Chemosphere 236:124308. https://doi.org/10.1016/j.chemosphere.2019.07.039
Kim E, Watanabe A, Sato R, Okajima K, Minagawa J (2019) pH-responsive binding properties of light-harvesting complexes in a photosystem II supercomplex investigated by thermodynamic dissociation kinetics analysis. J Phys Chem Lett 10:3615–3620. https://doi.org/10.1021/acs.jpclett.9b01208
Kučerová D, Labancová E, Vivodová Z, Kollárová K (2020) The modulation of ion homeostasis by silicon in cadmium treated poplar callus cells. Environ Sci Pollut Res 27:2857–2867. https://doi.org/10.1007/s11356-019-07054-1
Kumar S, Kalita A, Srivastava R, Sahoo L (2017) Co-expression of Arabidopsis NHX1 and bar improves the tolerance to salinity, oxidative stress, and herbicide in transgenic mungbean. Front Plant Sci 8:1896
Lan X-Y, He Q-S, Yang B, Yan Y-Y, Li X-Y, Xu F-L (2020) Influence of Cd exposure on H+ and Cd2+ fluxes in the leaf, stem and root of a novel aquatic hyperaccumulator - Microsorum pteropus. Chemosphere 249:126552. https://doi.org/10.1016/j.chemosphere.2020.126552
León Cañedo JA, Alarcón Silvas SG, Fierro Sañudo JF, Rodríguez M, de Oca GA, Partida Ruvalcaba L, Díaz Valdés T, Páez Osuna F (2019) Mercury and other trace metals in lettuce (Lactuca sativa) grown with two low-salinity shrimp effluents: Accumulation and human health risk assessment. Sci Total Environ 650:2535–2544. https://doi.org/10.1016/j.scitotenv.2018.10.003
León-Romero MA, Soto-Ríos PC, Fujibayashi M, Nishimura O (2017) Impact of NaCl solution pretreatment on plant growth and the uptake of multi-heavy metal by the model plant Arabidopsis thaliana. Water Air Soil Pollut 228:64. https://doi.org/10.1007/s11270-017-3241-8
Li C, Wei Z, Liang D, Zhou S, Li Y, Liu C, Ma F (2013) Enhanced salt resistance in apple plants overexpressing a Malus vacuolar Na+/H+ antiporter gene is associated with differences in stomatal behavior and photosynthesis. Plant Physiol Biochem 70:164–173. https://doi.org/10.1016/j.plaphy.2013.05.005
Li N, Wang X, Ma B, Du C, Zheng L, Wang Y (2017) Expression of a Na+/H+ antiporter RtNHX1 from a recretohalophyte Reaumuria trigyna improved salt tolerance of transgenic Arabidopsis thaliana. J Plant Physiol 218:109–120. https://doi.org/10.1016/j.jplph.2017.07.015
Li C, Yang X, Xu Y, Li L, Wang Y (2018) Cadmium detoxification induced by salt stress improves cadmium tolerance of multi-stress-tolerant Pichia kudriavzevii. Environ Pollut 242:845–854. https://doi.org/10.1016/j.envpol.2018.07.058
Li Q, Wang G, Guan C, Yang D, Wang Y, Zhang Y, Ji J, Jin C, An T (2019) Overexpression of LcSABP, an orthologous gene for salicylic acid binding protein 2, enhances drought stress tolerance in transgenic tobacco. Front Plant Sci 10:200
Li Q, Wang G, Wang Y, Dan Y, Guan C, Ji J (2019) Foliar application of salicylic acid alleviate the cadmium toxicity by modulation the reactive oxygen species in potato. Ecotoxicol Environ Saf 172:317–325. https://doi.org/10.1016/j.ecoenv.2019.01.078
Lin Y, Huang JJ, Dahms HU, Zhen JJ, Ying XP (2017) Cell damage and apoptosis in the hepatopancreas of Eriocheir sinensis induced by cadmium. Aquat Toxicol 190:190–198. https://doi.org/10.1016/j.aquatox.2017.07.008
Lin Y, Ying W, Na L, Jianyao Z, Yujie H, Zhaojiang Z, Sutong W, Yerong Z, Ying Z, Jinsheng S, Yong W (2019) Declined cadmium accumulation in Na+/H+ antiporter (NHX1) transgenic duckweed under cadmium stress. Ecotoxicol Environ Saf 182:109397. https://doi.org/10.1016/j.ecoenv.2019.109397
Liu Z, He X, Chen W, Yuan F, Yan K, Tao D (2009) Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator-Lonicera japonica Thunb. J Hazard Mater 169:170–175. https://doi.org/10.1016/j.jhazmat.2009.03.090
Liu Z, Ding Y, Wang F, Ye Y, Zhu C (2016) Role of salicylic acid in resistance to cadmium stress in plants. Plant Cell Rep 35:719–731. https://doi.org/10.1007/s00299-015-1925-3
Ma XL, Zhang Q, Shi HZ, Zhu JK, Zhao YX, Ma CL, Zhang H (2004) Molecular cloning and different expression of a vacuolar Na+/H+ antiporter gene in Suaeda salsa under salt stress. Biol Plant 48:219–225. https://doi.org/10.1023/B:BIOP.0000033448.96998.44
Mariem W, Kilani BR, Benet G, Abdelbasset L, Stanley L, Charlotte P, Chedly A, Tahar G (2014) How does NaCl improve tolerance to cadmium in the halophyte Sesuvium portulacastrum? Chemosphere 117:243–250. https://doi.org/10.1016/j.chemosphere.2014.07.041
Marschner H (2012) Preface to First Edition. In: P Marschner (ed) Marschner's Mineral Nutrition of Higher Plants (3rd edn). Academic, San Diego
Mei X, Li S, Li Q, Yang Y, Luo X, He B, Li H, Xu Z (2014) Sodium chloride salinity reduces Cd uptake by edible amaranth (Amaranthus mangostanus L.) via competition for Ca channels. Ecotoxicol Environ Saf 105:59–64. https://doi.org/10.1016/j.ecoenv.2014.04.005
Mesnoua M, Mateos-Naranjo E, Barcia-Piedras JM, Pérez-Romero JA, Lotmani B, Redondo-Gómez S (2016) Physiological and biochemical mechanisms preventing Cd-toxicity in the hyperaccumulator Atriplex halimus L. Plant Physiol Biochem 106:30–38. https://doi.org/10.1016/j.plaphy.2016.04.041
Mishra B, Sangwan RS, Mishra S, Jadaun JS, Sabir F, Sangwan NS (2014) Effect of cadmium stress on inductive enzymatic and nonenzymatic responses of ROS and sugar metabolism in multiple shoot cultures of Ashwagandha (Withania somnifera Dunal). Protoplasma 251:1031–1045. https://doi.org/10.1007/s00709-014-0613-4
Nam Y-J, Tran L-SP, Kojima M, Sakakibara H, Nishiyama R, Shin R (2012) Regulatory roles of cytokinins and cytokinin signaling in response to potassium deficiency in Arabidopsis. PLoS One 7:e47797. https://doi.org/10.1371/journal.pone.0047797
Nawaz I, Iqbal M, Hakvoort HWJ, Bliek M, de Boer B, Schat H (2014) Expression levels and promoter activities of candidate salt tolerance genes in halophytic and glycophytic Brassicaceae. Environ Exp Bot 99:59–66. https://doi.org/10.1016/j.envexpbot.2013.10.006
Pompeu GB, Ambrosano GB, Vilhena MB, Carvalho RF, Gratão PL, Andrino F, Lira SPd, Azevedo RA (2019) Potential of hydrogen (pH) differentially modulates cadmium stress response in abscisic acid-deficient sitiens tomato mutant. Bragantia 78:317–327
Rehman S, Abbas G, Shahid M, Saqib M, Umer Farooq AB, Hussain M, Murtaza B, Amjad M, Naeem MA, Farooq A (2019) Effect of salinity on cadmium tolerance, ionic homeostasis and oxidative stress responses in conocarpus exposed to cadmium stress: Implications for phytoremediation. Ecotoxicol Environ Saf 171:146–153. https://doi.org/10.1016/j.ecoenv.2018.12.077
Rodríguez-Rosales MP, Jiang X, Gálvez FJ, Aranda MN, Cubero B, Venema K (2008) Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol 179:366–377. https://doi.org/10.1111/j.1469-8137.2008.02461.x
Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229. https://doi.org/10.1104/pp.108.131524
Sahoo DP, Kumar S, Mishra S, Kobayashi Y, Panda SK, Sahoo L (2016) Enhanced salinity tolerance in transgenic mungbean overexpressing Arabidopsis antiporter (NHX1) gene. Mol Breed 36:144. https://doi.org/10.1007/s11032-016-0564-x
Schmidt FJ, Zimmermann MM, Wiedmann DR, Lichtenauer S, Grundmann L, Muth J, Twyman RM, Prüfer D, Noll GA (2020) The major floral promoter NtFT5 in tobacco (Nicotiana tabacum) is a promising target for crop improvement. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.01666
Shavrukov Y (2012) Salt stress or salt shock: which genes are we studying? J Exp Bot 64:119–127. https://doi.org/10.1093/jxb/ers316
Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357. https://doi.org/10.1093/pcp/pci145
Sottosanto JB, Saranga Y, Blumwald E (2007) Impact of AtNHX1, a vacuolar Na+/H+ antiporter, upon gene expression during short- and long-term salt stress in Arabidopsis thaliana. BMC Plant Biol 7:18. https://doi.org/10.1186/1471-2229-7-18
Van Belleghem F, Cuypers A, Semane B, Smeets K, Vangronsveld J, d’Haen J, Valcke R (2007) Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana. New Phytol 173:495–508. https://doi.org/10.1111/j.1469-8137.2006.01940.x
Venema K, Quintero FJ, Pardo JM, Donaire JP (2002) The Arabidopsis Na+/H+ exchanger AtNHX1 catalyzes low affinity Na+ and K+ transport in reconstituted liposomes. J Biol Chem 277:2413–2418
Wali M, Gunsè B, Llugany M, Corrales I, Abdelly C, Poschenrieder C, Ghnaya T (2016) High salinity helps the halophyte Sesuvium portulacastrum in defense against Cd toxicity by maintaining redox balance and photosynthesis. Planta 244:333–346. https://doi.org/10.1007/s00425-016-2515-5
Wang X, Cheng M, Yang Q, Wei H, Xia A, Wang L, Ben Y, Zhou Q, Yang Z, Huang X (2019) A living plant cell-based biosensor for real-time monitoring invisible damage of plant cells under heavy metal stress. Sci Total Environ 697:134097. https://doi.org/10.1016/j.scitotenv.2019.134097
Wiszniewska A, Koźmińska A, Hanus-Fajerska E, Dziurka M, Dziurka K (2019) Insight into mechanisms of multiple stresses tolerance in a halophyte Aster tripolium subjected to salinity and heavy metal stress. Ecotoxicol Environ Saf 180:12–22. https://doi.org/10.1016/j.ecoenv.2019.04.059
Wu CA, Yang GD, Meng QW, Zheng CC (2004) The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an iportant role in salt stress. Plant Cell Physiol 45:600–607. https://doi.org/10.1093/pcp/pch071
Wu G, Wang G, Ji J, Li Y, Gao H, Wu J, Guan W (2015) A chimeric vacuolar Na+/H+ antiporter gene evolved by DNA family shuffling confers increased salt tolerance in yeast. J Biotechnol 203:1–8. https://doi.org/10.1016/j.jbiotec.2015.02.033
Xue Z, Zhi D, Xue G, Zhang H, Zhao Y, Xia G (2004) Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Sci 167:849–859. https://doi.org/10.1016/j.plantsci.2004.05.034
Yamaguchi T, Fukada-Tanaka S, Inagaki Y, Saito N, Yonekura-Sakakibara K, Tanaka Y, Kusumi T, Iida S (2001) Genes encoding the vacuolar Na+/H+ exchanger and flower coloration. Plant Cell Physiol 42:451–461. https://doi.org/10.1093/pcp/pce080
Yang L, Han Y, Wu D, Yong W, Liu M, Wang S, Liu W, Lu M, Wei Y, Sun J (2017) Salt and cadmium stress tolerance caused by overexpression of the Glycine Max Na+/H+ Antiporter (GmNHX1) gene in duckweed (Lemna turionifera 5511). Aquat Toxicol 192:127–135. https://doi.org/10.1016/j.aquatox.2017.08.010
Zeng L, Zhu T, Gao Y, Wang Y, Ning C, Björn LO, Chen D, Li S (2017) Effects of Ca addition on the uptake, translocation, and distribution of Cd in Arabidopsis thaliana. Ecotoxicol Environ Saf 139:228–237. https://doi.org/10.1016/j.ecoenv.2017.01.023
Zhang BL, Shang SH, Jabeen Z, Zhang GP (2014) Involvement of ethylene in alleviation of Cd toxicity by NaCl in tobacco plants. Ecotoxicol Environ Saf 101:64–69. https://doi.org/10.1016/j.ecoenv.2013.12.013
Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252:911–924. https://doi.org/10.1007/s00709-014-0732-y
Zhang WD, Wang P, Bao Z, Ma Q, Duan LJ, Bao AK, Zhang JL, Wang SM (2017) SOS1, HKT1;5, and NHX1 snergistically modulate Na+ homeostasis in the halophytic grass Puccinellia tenuiflora. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00576
Zhao N, Zhu H, Zhang H, Sun J, Zhou J, Deng C, Zhang Y, Zhao R, Zhou X, Lu C, Lin S, Chen S (2018) Hydrogen sulfide mediates K+ and Na+ homeostasis in the roots of salt-resistant and salt-sensitive poplar species subjected to NaCl stress. Front Plant Sci 9:1366
Zhou MX, Han RM, Ghnaya T, Lutts S (2018) Salinity influences the interactive effects of cadmium and zinc on ethylene and polyamine synthesis in the halophyte plant species Kosteletzkya pentacarpos. Chemosphere 209:892–900. https://doi.org/10.1016/j.chemosphere.2018.06.143
Zhou M, Renard M, Quinet M, Lutts S (2019) Effect of NaCl on proline and glycinebetaine metabolism in Kosteletzkya pentacarpos exposed to Cd and Zn toxicities. Plant Soil 441:525–542. https://doi.org/10.1007/s11104-019-04143-5
Zoufan P, Azad Z, Rahnama Ghahfarokhie A, Kolahi M (2020) Modification of oxidative stress through changes in some indicators related to phenolic metabolism in Malva parviflora exposed to cadmium. Ecotoxicol Environ Saf 187:109811. https://doi.org/10.1016/j.ecoenv.2019.109811
Acknowledgments
Tianjin Science and Technology Research and Development Plan Project (19YFZCSN00280) and Tianjin Rice Industry Technology System Innovation Team Construction (ITTRRS2018007).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There are no conflicts of interest.
Additional information
Responsible editor: Ricardo Aroca
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOC 15 kb)
Rights and permissions
About this article
Cite this article
Wang, G., Yang, D., Zhang, Y. et al. Na+/H+ antiporter (NHX1) positively enhances cadmium (Cd) resistance and decreases Cd accumulation in tobacco plants cultivated in Cd-containing soil. Plant Soil 453, 389–408 (2020). https://doi.org/10.1007/s11104-020-04601-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04601-5