The responses of Ca2+ signaling mechanism to salt stress in pears are poorly understood. In this study, we investigated the difference in the Ca2+ signal responses to NaCl stress in two pear species (Pyrus betulaefolia Bunge. and P. bretschneideri Rehd. cv. ‘Xuehua’). Pear protoplasts were treated with 100 mM NaCl alone and NaCl combined with various chemical agents before changes in intracellular Ca2+ levels and the expression of Ca2+ sensor-related genes were analyzed. NaCl stress caused elevated Ca2+ levels in protoplasts labeled with the calcium indicator Fluo-3/AM. The Ca2+ signal increased earlier in P. betulaefolia than in the ‘Xuehua’ cultivar. The cytoplasmic Ca2+ bursts induced by NaCl stress were significantly constrained by the chemical agents supplied to both species. The plasma-membrane Ca2+ channel inhibitor LaCl3 and extracellular Ca2+ chelator EGTA had greater inhibitory effects than the intracellular Ca2+ chelator BAPTA/AM. Under NaCl stress, upregulation of PbCBL10 and genes in the classes PbCDPK and PbCIPK occurred more quickly in P. betulaefolia than the ‘Xuehua’ cultivar. In conclusion, NaCl stress stimulates Ca2+ signaling in pear cells, the ions for which are taken from extracellular and intracellular Ca2+ stores. Furthermore, the accumulation of cytoplasmic Ca2+ mediates early expression of Ca2+ sensor-related genes, especially PbCDPK1. Thus the response of Ca2+ signal plays pivotal roles, which enhance the salt tolerance of pear.
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Szabo, S., Hossain, M.S., Adger, W.N., Matthews, Z., Ahmed, S., Lázár, A.N., and Ahmad, S., Soil salinity, household wealth and food insecurity in tropical deltas: evidence from south-west coast of Bangladesh, Sustain. Sci., 2016, vol. 11, p. 411.
Liang, W., Ma, X., Wan, P., and Liu, L., Plant salt-tolerance mechanism: a review, Biochem. Biophys. Res. Commun., 2018, vol. 495, p. 286.
Elkelish, A.A., Alnusaire, T.S., Soliman, M.H., Gowayed, S., Senousy, H.H., and Fahad, S., Calcium availability regulates antioxidant system, physio-biochemical activities and alleviates salinity stress mediated oxidative damage in soybean seedlings, J. Appl. Bot. Food Qual., 2019, p. 258.
Bush, D.S., Effects of gibberellic acid and environmental factors on cytosolic calcium in wheat aleurone cells, Planta, 1996, vol. 199, p. 89.
Pauly, N., Knight, M. R., Thuleau, P., Graziana, A., Muto, S., Ranjeva, R. and Mazars, C., The nucleus together with the cytosol generates patterns of specific cellular calcium signatures in tobacco suspension culture cells, Cell Calcium, 2001, vol. 30, p. 413.
Stael, S., Wurzinger, B., Mair, A., Mehlmer, N., Vothknecht, U.C., and Teige, M., Plant organellar calcium signalling: an emerging field, J. Exp. Bot., 2012, vol. 63, p. 1525.
Dubrovina, A.S., Aleynova, O.A., Ogneva, Z.V., Suprun, A.R., Ananev, A.A., and Kiselev, K.V., The effect of abiotic stress conditions on expression of calmodulin (CaM) and calmodulin-like (CML) genes in wild-growing grapevine Vitis amurensis, Plants, 2019, vol. 8, p. 602.
Qiu, Q., Guo, Y., Dietrich, M.A., Schumaker K.S., and Zhu, J., Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, p. 8436.
Ma, L., Ye, J., Yang Y., Lin, H., Yue, L., Luo, J., Yu, L., Fu, H., and Liu, X., The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress, Dev. Cell, 2019, vol. 48, p. 697.
Ma, S. and Wu, W., AtCPK23 functions in Arabidopsis responses to drought and salt stresses, Plant Mol. Biol., 2007, vol. 65, p. 511.
Dubrovina, A.S. and Kiselev, K.V., The role of calcium-dependent protein kinase genes VaCPK1 and VaCPK26 in the response of Vitis amurensis (in vitro) and Arabidopsis thaliana (in vivo) to abiotic stresses, Russ. J. Genet., 2019, vol. 55, p. 319.
Tang, J., Lin, J., Li, H., Li, X, Yang, Q., Cheng, Z., and Chang, Y., Characterization of CIPK family in Asian pear (Pyrus bretschneideri Rehd) and co-expression analysis related to salt and osmotic stress responses, Front. Plant Sci., 2016, vol. 7, p. 1361.
Okubo, M., Furukawa, Y., and Sakuratani, T., Growth, flowering and leaf properties of pear cultivars grafted on two Asian pear rootstock seedlings under NaCl irrigation, Sci. Hortic., 2000, vol. 85, p. 91.
Duan, Y., Tian, C., Song Y., and Li L., In vitro culture and rapid propagation of ‘Xuehua’ pear, J. Shanxi Agri-c. Univ., Nat. Sci. Ed., 2014, vol. 34, p. 464.
Pan, Z., Studies on the culture, regeneration and fusion of protoplast in apple, Extended Abstract of Cand. Sci. (Biol.) Dissertation, PhD Thesis, Wuhan: Huazhong Agricu-ltural Univ., 1998.
Horváth, E., Protoplast isolation from Solanum lycope-rsicum L. leaf tissues and their response to short-term NaCl treatment, Acta Biol. Szeged, 2009, vol. 53, p. 83.
Liu, Y., Wang, Y., Li, J., and Li, L., Responses of intracellular Ca2+ and its sensors to Venturia nashicola infection in pear (Pyrus bretschneideri) with differing resistance, Sci. Hortic., 2019, vol. 243, p. 552.
Chang, S., Puryear, J., and Cairney, J., A simple and efficient method for isolating RNA from pine trees, Plant Mol. Biol. Rep., 1993, vol. 11, p. 113.
Livaka, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method, Methods, 2001, vol. 25, p. 402.
Tang, J., Lin, J., Li, X., Yang, Q., Cheng, Q., Cheng, Z., and Chang, Y., Characterization and expression profiling analysis of calmodulin genes in response to salt and osmotic stresses in pear (Pyrus bretschneideri Rehd.) and in comparison with Arabidopsis, BioMed Res. Int., 2017, vol. 2017: 7904162.
Xu, Y., Lin, J., Li, X., and Chang, Y., Identification and expression analysis under abiotic stresses of the CBL gene family in pear, Sci. Agric. Sin., 2015, vol. 48, p. 735.
Sun, J, Wang, M., Ding, M., Deng, S., Liu, M., Lu, C., Zhou, X., Shen, X., Zheng, X., and Zhang, Z., H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells, Plant Cell Enviro-n., 2010, vol. 32, p. 943.
Mohammed, A., Kader, S.L., Thorsten, S., Dortje G., and Yemelyanov, V., Sodium sensing induces different changes in free cytosolic calcium concentration and pH in salt-tolerant and -sensitive rice (Oryza sativa) cultivars, Physiol. Plant., 2007, vol. 130, p. 99.
Knight, H., Trewavas, A.J., and Knight, M.R., Calcium signalling in Arabidopsis thaliana responding to drought and salinity, Plant J., 1997, vol. 12, p. 1067.
Zhang, X., Shen, Z., Sun, J., Yu, Y., Deng, S., Li, Z., Sun, C., Zhang, J., Zhao, R., Shen, X., and Chen, S., NaCl-elicited, vacuolar Ca2+ release facilitates prolonged cytosolic Ca2+ signaling in the salt response of Populus euphratica cells, Cell Calcium, 2015, vol. 57, p. 348.
Yuenyon, W., Chinpongpanich, A., Comai, L., Chadchawan, S., and Buaboocha, T., Downstream components of the calmodulin signaling pathway in the rice salt stress response revealed by transcriptome profiling and target identification, BMC Plant Biol., 2018, vol. 18, p. 335.
Zhou, S., Jia, L., Chu, H., Wu, D., Peng, X., Liu, X., Zhang, J., and Zhao, J., Arabidopsis CaM1 and CaM4 promote nitric oxide production and salt resistance by inhibiting S-nitrosoglutathione reductase via direct binding, PLoS Genet., 2016, vol. 12: e1006255.
Dubrovina, A.S., Kiselev, K.V., and Khristenko, V.S., Expression of calcium-dependent protein kinase (CDPK) genes under abiotic stress conditions in wild-growing grapevine Vitis amurensis, Plant Physiol., 2013, vol. 170, p. 1494.
Yang, Y., Zhang, C., Tang, R., Xu, H., and Lan, W., Calcineurin B-like proteins CBL4 and CBL10 mediate two independent salt tolerance pathways in Arabidopsis, Int. J. Mol. Sci., 2019, vol. 20, p. 2421.
Nath, M., Bhatt, D., Jain, A., Saxena, S.C., Saifi, S.K., Yadav, S., Negi, M., Prasad, R., and Tuteja, N., Salt stress triggers augmented levels of Na+, Ca2+ and ROS and alter stress responsive gene expression in roots of CBL9 and CIPK23 knockout mutants of Arabidopsis thaliana, Environ. Exp. Bot., 2019, vol. 161, p. 265.
This work was supported by the Key Project of the Key Research and Development Program of Shanxi Province, China (project nos. 201703D 221015-2 and 201703D211001).
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants as objects of research.
Abbreviations: 6-BA—6-benzylaminopurine; CaM—calmodulin, CBL—calcineurin B-like protein; CDPK—calcium-dependent protein kinase; CIPK—CBL-interacting protein kinase; CPW—cell protoplast wash; FDA—fluorescein diacetate; IBA—indole-3-butytric acid; LaCl3—lanthanum chloride; SOS—salt-overly-sensitive.
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Li, J., Xie, B., Liu, Y. et al. Changes to Intracellular Ca2+ and Its Sensors Triggered by NaCl Stress in Pears. Russ J Plant Physiol 67, 1144–1151 (2020). https://doi.org/10.1134/S1021443720060126
- Pyrus betulaefolia
- Pyrus bretschneideri
- NaCl stress
- cytoplasmic Ca2+
- Ca2+ sensor -related genes