Abstract
This study aimed to explore the mechanism by which calcium (Ca) signal regulated carbohydrate metabolism and exogenous Ca alleviated salinity toxicity. Wheat seedlings were treated with sodium chloride (NaCl, 150 mM) alone or combined with 500 μM calcium chloride (CaCl2), lanthanum chloride (LaCl3) and/or ethylene glycol tetraacetic acid (EGTA) to primarily analyse carbohydrate starch and sucrose metabolism, as well as Ca signaling components. Treatment with NaCl, EGTA, or LaCl3 alone retarded wheat-seedling growth and decreased starch content accompanied by weakened ribulose-1,5-bisphosphate carboxylation/oxygenase (Rubisco) and Rubisco activase activities, as well as enhanced glyceraldehyde-3-phosphate dehydrogenase, phosphoglycerate kinase, alpha-amylase, and beta-amylase activities. However, it increased the sucrose level, up-regulated the sucrose phosphate synthase (SPS) and sucrose synthase (SuSy) activities and TaSPS and TaSuSy expression together, but down-regulated the acid invertase (SA-Inv) and alkaline/neutral invertase (A/N-Inv) activities and TaSA-Inv and TaA/N-Inv expression. Except for unchanged A/N-Inv activities and TaA/N-Inv expression, adding CaCl2 effectively blocked the sodium salt-induced changes of these parameters, which was partially eliminated by EGTA or LaCl3 presence. Furthermore, NaCl treatment also significantly inhibited Ca-dependent protein kinases and Ca2+-ATPase activities and their gene expression in wheat leaves, which was effectively relieved by adding CaCl2. Taken together, CaCl2 application effectively alleviated the sodium salt-induced retardation of wheat-seedling growth by enhancing starch anabolism and sucrose catabolism, and intracellular Ca signal regulated the enzyme activities and gene expression of starch and sucrose metabolism in the leaves of sodium salt-stressed wheat seedlings.
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References
Bachani J, Mahanty A, Aftab T, Kumar K (2022) Insight into calcium signalling in salt stress response. S Afr J Bot 151:1–8. https://doi.org/10.1016/j.sajb.2022.09.033
Bai QY, Yang RQ, Zhang LX, Gu ZX (2013) Salt stress induces accumulation of γ–aminobutyric acid in germinated foxtail millet (Setaria italica L.). Cereal Chem 90(2):145–149. https://doi.org/10.1094/CCHEM-06-12-0071-R
ElSayed AI, Mohamed AH, Rafudeen MS, Omar AA, Awad MF, Mansour E (2022) Polyamines mitigate the destructive impacts of salinity stress by enhancing photosynthetic capacity, antioxidant defense system and upregulation of Calvin cycle-related genes in rapeseed (Brassica napus L.). Saudi J Biol Sci 29(5):3675–3686. https://doi.org/10.1016/J.SJBS.2022.02.053
Gao JF (2006) Experimental supervision of plant physiology. Beijing, pp 100–103
Gao YL, Long RC, Kang JM, Wang Z, Zhang TJ, Sun H, Li X, Yang QC (2019) Comparative proteomic analysis reveals that antioxidant system and soluble sugar metabolism contribute to salt tolerance in alfalfa (Medicago sativa L.) leaves. J Proteome Res 18(1):191–203. https://doi.org/10.1021/acs.jproteome.8b00521
Hajihashemi S, Skalicky M, Brestic M, Pavla V (2020) Cross-talk between nitric oxide, hydrogen peroxide and calcium in salt-stressed Chenopodium quinoa Willd. at seed germination stage. Plant Physiol Biochem 154:657–664. https://doi.org/10.1016/j.plaphy.2020.07.022
Hu T, Hu LX, Zhang XZ, Zhang PP, Zhao ZJ, Fu JM (2013) Differential responses of CO2 assimilation, carbohydrate allocation and gene expression to NaCl stress in perennial ryegrass with different salt tolerance. PLoS ONE 8(6):e66090. https://doi.org/10.1371/journal.pone.0066090
Hu W, Loka DA, Fitzsimons TR, Zhou ZG, Oosterhuis DM (2018) Potassium deficiency limits reproductive success by altering carbohydrate and protein balances in cotton (Gossypium hirsutum L.). Environ Exp Bot 145:87–94. https://doi.org/10.1016/j.envexpbot.2017.10.024
Huang GY, Shan CJ (2018) Lanthanum improves the antioxidant capacity in chloroplast of tomato seedlings through ascorbate-glutathione cycle under salt stress. Sci Hortic 232:264–268. https://doi.org/10.1016/j.scienta.2018.01.025
Huang K, Peng L, Liu YY, Yao RD, Liu ZB, Li XF, Yang L, Wang JM (2018) Arabidopsis calcium-dependent protein kinase AtCPK1 plays a positive role in salt/drought-stress response. Biochem Biophys Res Commun 498(1):92–98. https://doi.org/10.1016/j.bbrc.2017.11.175
Ju FY, Pang JL, Huo YY, Zhu JJ, Yu K, Sun LY, Loka DA, Hu W, Zhou ZG, Wang SS, Chen BL, Tang QX (2021) Potassium application alleviates the negative effects of salt stress on cotton (Gossypium hirsutum L.) yield by improving the ionic homeostasis, photosynthetic capacity and carbohydrate metabolism of the leaf subtending the cotton boll. Field Crops Res 272:108288. https://doi.org/10.1016/J.FCR.2021.108288
Kamran M, Wang D, Xie KZ, Lu YS, Shi CH, EL Sabagh A, Gu WJ, Xu PZ (2021) Pre-sowing seed treatment with kinetin and calcium mitigates salt induced inhibition of seed germination and seedling growth of choysum (Brassica rapa var. Parachinensis). Ecotoxicol Environ Saf 227:112921. https://doi.org/10.1016/j.ecoenv.2021.112921
Ke QB, Ye J, Wang BM, Ren JH, Yin LN, Deng XP, Wang SW (2018) Melatonin mitigates salt stress in wheat seedlings by modulating polyamine metabolism. Front Plant Sci 9:914. https://doi.org/10.3389/fpls.2018.00914
Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40(2):482–487. https://doi.org/10.2135/cropsci2000.402482x
Kumar RR, Goswami S, Singh K, Dubey K, Singh S, Sharma R, Verma N, Kala YK, Rai GK, Grover M, Mishra DC, Singh B, Pathak H, Chinnusamy V, Rai A, Praveen S (2016) Identification of putative Rubisvo activase (TaRca1)-The catalytic chaperone regulating carbon assimilatory pathway in wheat (Triticum aestivum) under the heat stress. Front Plant Sci 7:986. https://doi.org/10.3389/fpls.2016.00986
Li XN, Jiang HD, Liu FL, Cai J, Dai TB, Cao WX, Jiang D (2013) Induction of chilling tolerance in wheat during germination by pre-soaking seed with nitric oxide and gibberellin. Plant Growth Regul 71:31–40. https://doi.org/10.1007/s10725-013-9805-8
Li Y, Fang F, Guo F, Meng JJ, Li XG, Xia GM, Wan SB (2014) Isolation and functional characterisation of CDPKs gene from Arachis hypogaea under salt stress. Funct Plant Biol 42(3):274–283. https://doi.org/10.1071/FP14190
Li CH, Li YH, Chu PY, Hao-hao Z, Wei ZM, Cheng Y, Liu XX, Zhao FZ, Li Y-J, Zhang ZW, Zheng Y, Mu ZS (2022a) Effects of salt stress on sucrose metabolism and growth in Chinese rose (Rosa chinensis). Biotechnol Biotechnol Equip 36(1):706–716. https://doi.org/10.1080/13102818.2022.2116356
Li Q, Liu R, Li ZH, Fan H, Song J (2022b) Positive effects of NaCl on the photoreaction and carbon assimilation efficiency in Suaeda salsa. Plant Physiol Biochem 177:32–37. https://doi.org/10.1016/J.PLAPHY.2022.02.019
Li SX, Wang Y, Gao XQ, Lan J, Fu BZ (2022c) Comparative physiological and transcriptome analysis reveal the molecular mechanism of melatonin in regulating salt tolerance in alfalfa (Medicago sativa L.). Front Plant Sci 13:919177. https://doi.org/10.3389/FPLS.2022.919177
Li Y, Chu Y, Yao K, Shi C, Deng X, Lin J (2023) Response of sugar metabolism in the cotyledons and roots of Ricinus communis subjected to salt stress. Plant Biol 25(1):62–71. https://doi.org/10.1111/plb.13475
Liu JR, Ma YN, Lv FJ, Chen J, Zhou ZG, Wang YH, Abudurezike A, Oosterhuis DM (2013) Changes of sucrose metabolism in leaf subtending to cotton boll under cool temperature due to late planting. Field Crop Res 144:200–211. https://doi.org/10.1016/j.fcr.2013.02.003
Liu W, Yuan XT, Zhang YY, Xuan YN, Yan YQ (2014) Effects of salt stress and exogenous Ca2+ on Na+ compartmentalization, ion pump activities of tonoplast and plasma membrane in Nitraria tangutorum Bobr. leaves. Acta Physiol Plant 36:2183–2193. https://doi.org/10.1007/s11738-014-1595-8
Liu L, Wang B, Liu D, Zou CL, Wu PR, Wang ZY, Wang YB, Li CF (2020) Transcriptomic and metabolomic analyses reveal mechanisms of adaptation to salinity in which carbon and nitrogen metabolism is altered in sugar beet roots. BMC Plant Biol 20:138. https://doi.org/10.1186/s12870-020-02349-9
Lu QH, Wang YQ, Yang HB (2021) Effect of exogenous calcium on physiological characteristics of salt tolerance in Tartary buckwheat. Biologia 76:3621–3630. https://doi.org/10.1007/s11756-021-00904-9
Ma Y, Wang P, Gu ZX, Tao Y, Shen C, Zhou YL, Han YB, Yang RQ (2019) Ca2+ involved in GABA signal transduction for phenolics accumulation in germinated hulless barley under NaCl stress. Food Chem X 2:100011–100023. https://doi.org/10.1016/j.fochx.2019.100023
Manishankar P, Wang NL, Köster P, Alatar AA, Kudla J (2018) Calcium signaling during salt stress and in the regulation of ion homeostasis. J Exp Bot 69(17):4215–4226. https://doi.org/10.1093/jxb/ery201
Meng FY, Feng NJ, Zheng DF, Liu ML, Zhang RJ, Huang XX, Huang AQ, Chen ZM (2023) Exogenous Hemin alleviates NaCl stress by promoting photosynthesis and carbon metabolism in rice seedlings. Sci Rep 13:3497. https://doi.org/10.1038/s41598-023-30619-7
Miceli A, Moncada A, Vetrano F (2021) Use of microbial biostimulants to increase the salinity tolerance of vegetable transplants. Agronomy 11(6):1143. https://doi.org/10.3390/agronomy11061143
Nawaz H, Manhalter S, Ali A, Ashraf MY, Lang I (2019) Ni tolerance and its distinguished amelioration by chelating agents is reflected in root radius of B. napus cultivars. Protoplasma 256:171–179. https://doi.org/10.1007/s00709-018-1287-0
Nitsche J, Josts I, Heidemann J, Mertens HD, Maric S, Moulin M, Haertlein M, Busch S, Forsyth VT, Svergun DI, Uetrecht C, Tidow H (2018) Structural basis for activation of plasma-membrane Ca2+-ATPase by calmodulin. Commun Biol 1:206. https://doi.org/10.1038/s42003-018-0203-7
Pan JW, Li Z, Wang QG, Guan YN, Li XB, Huangfu YG, Meng FH, Li JL, Dai SJ, Liu W (2021) Phosphoproteomic profiling reveals early salt-responsive mechanisms in two foxtail millet cultivars. Front Plant Sci 12:712257. https://doi.org/10.3389/FPLS.2021.712257
Patel A, Tiwari S, Prasad SM (2023) Modulation of salt stress in paddy field cyanobacteria with exogenous application of gibberellic acid: growth behavior and antioxidative status. Physiol Mol Biol Plants 29(1):51–68. https://doi.org/10.1007/s12298-022-01266-5
Qi NN, Wang N, Hou XM, Li YH, Liao WB (2022) Involvement of calcium and calmodulin in NO-alleviated salt stress in tomato seedlings. Plants 11(19):2479. https://doi.org/10.3390/plants11192479
Qiu NW, Liu Q, Li JJ, Zhang YH, Wang FD, Gao JW (2017) Physiological and transcriptomic responses of Chinese cabbage (Brassica rapa L. ssp. pekinensis) to salt stress. Int J Mol Sci 18(9):1953. https://doi.org/10.3390/ijms18091953
Rekowski A, Langenkämper G, Dier M, Wimmer MA, Scherf KA, Zörb C (2021) Determination of soluble wheat protein fractions using the Bradford assay. Cereal Chem 98(5):1059–1065. https://doi.org/10.1002/cche.10447
Roy PR, Tahjib-Ul-Arif M, Polash MAS, Hossen MZ, Hossain MA (2019) Physiological mechanisms of exogenous calcium on alleviating salinity-induced stress in rice (Oryza sativa L.). Physiol Mol Biol Plants 25(3):611–624. https://doi.org/10.1007/s12298-019-00654-8
Seckin Dinler B, Cetinkaya H, Secgin Z (2023) The regulation of glutathione s-transferases by gibberellic acid application in salt treated maize leaves. Physiol Mol Biol Plants 29(1):69–85. https://doi.org/10.1007/s12298-022-01269-2
Shen JL, Wang Y, Shu S, Jahan MS, Zhong M, Wu JQ, Sun J, Guo SR (2019) Exogenous putrescine regulates leaf starch overaccumulation in cucumber under salt stress. Sci Hortic 253:99–110. https://doi.org/10.1016/j.scienta.2019.04.010
Shu HM, Zhou ZG, Xu NY, Wang YH, Zheng M (2009) Sucrose metabolism in cotton (Gossypium hirsutum L.) fibre under low temperature during fibre development. Eur J Agron 31(2):61–68. https://doi.org/10.1016/j.eja.2009.03.004
Singh A, Roychoudhury A, Samanta S, Banerjee A (2021) Fluoride stress-mediated regulation of tricarboxylic acid cycle and sugar metabolism in rice seedlings in absence and presence of exogenous calcium. J Plant Growth Regul 40:1579–1593. https://doi.org/10.1007/s00344-020-10202-4
Sui N, Yang Z, Liu ML, Wang BS (2015) Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genomics 16:534. https://doi.org/10.1186/s12864-015-1760-5
Sze H, Liang F, Hwang I, Curran AC, Harper JF (2000) Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51:433–462. https://doi.org/10.1146/annurev.arplant.51.1.433
Valivand M, Amooaghaie R, Ahadi A (2019) Seed priming with H2S and Ca2+ trigger signal memory that induces cross-adaptation against nickel stress in zucchini seedlings. Plant Physiol Biochem 143:286–298. https://doi.org/10.1016/j.plaphy.2019.09.016
Vivek PJ, Tuteja N, Soniya EV (2013) CDPK1 from ginger promotes salinity and drought stress tolerance without yield penalty by improving growth and photosynthesis in Nicotiana tabacum. PLoS ONE 8(10):e76392. https://doi.org/10.1371/journal.pone.0076392
Wan SQ, Wang WD, Zhou TS, Zhang YH, Chen JF, Xiao B, Yang YJ, Yu YB (2018) Transcriptomic analysis reveals the molecular mechanisms of Camellia sinensis in response to salt stress. Plant Growth Regul 84:481–492. https://doi.org/10.1007/s10725-017-0354-4
Wang HB, Xie F, Yao YZ, Zhao B, Xiao QQ, Pan YH, Wang HJ (2012) The effects of arsenic and induced-phytoextraction methods on photosynthesis in Pteris species with different arsenic-accumulating abilities. Environ Exp Bot 75:298–306. https://doi.org/10.1016/j.envexpbot.2011.08.002
Wang XC, Chang LL, Wang BC, Wang D, Li PH, Wang LM, Yi XP, Huang QX, Peng M, Guo AP (2013) Comparative proteomics of Thellungiella halophila leaves from plants subjected to salinity reveals the importance of chloroplastic starch and soluble sugars in halophyte salt tolerance. Mol Cell Proteom 12(8):2174–2195. https://doi.org/10.1074/mcp.M112.022475
Wei MY, Liu JY, Li H, Hu WJ, Shen ZJ, Qiao F, Zhu CQ, Chen J, Liu X, Zheng HL (2021) Proteomic analysis reveals the protective role of exogenous hydrogen sulfide against salt stress in rice seedlings. Nitric Oxide 111–112:14–30. https://doi.org/10.1016/J.NIOX.2021.04.002
Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Plant Sci 19(1):31–67. https://doi.org/10.1080/07352680091139178
Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen ZX, Yu JQ (2009) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230:1185–1196. https://doi.org/10.1007/s00425-009-1016-1
Xing YF, Chen XF, Zhang M, Bang Li, Cui T, Liu C, Liu CJ, Chen BR, Zhou YF (2023) CaCl2 priming promotes sorghum seed germination under salt stress by activating sugar metabolism. Plant Growth Regul 101:385–397. https://doi.org/10.1007/s10725-023-01025-w
Xu ZS, Chen XJ, Lu XP, Zhao BP, Yang YM, Liu JH (2021) Integrative analysis of transcriptome and metabolome reveal mechanism of tolerance to salt stress in oat (Avena sativa L.). Plant Physiol Biochem 160:315–328. https://doi.org/10.1016/J.PLAPHY.2021.01.027
Yan FY, Zhang JY, Li WW, Ding YF, Zhong QY, Xu X, Wei HM, Li GH (2021) Exogenous melatonin alleviates salt stress by improving leaf photosynthesis in rice seedlings. Plant Physiol Biochem 163:367–375. https://doi.org/10.1016/J.PLAPHY.2021.03.058
Yang YL, Wei XL, Shi RY, Fan Q, An LZ (2010) Salinity-induced physiological modification in the callus from halophyte Nitraria tangutorum Bobr. J Plant Growth Regul 29:465–476. https://doi.org/10.1007/s00344-010-9158-8
Yang Y, Xie JM, Li J, Zhang J, Zhang XD, Yao YD, Wang C, Niu TH, Bakpa EP (2022) Trehalose alleviates salt tolerance by improving photosynthetic performance and maintaining mineral ion homeostasis in tomato plants. Front Plant Sci 13:974507. https://doi.org/10.3389/FPLS.2022.974507
Yu QL, Sun WJ, Han YY, Hao JH, Qin XX, Liu CJ, Fan SX (2022) Exogenous spermidine improves the sucrose metabolism of lettuce to resist high-temperature stress. Plant Growth Regul 96:497–509. https://doi.org/10.1007/S10725-022-00800-5
Zhang LN, Xie JQ, Wang LT, Si LB, Zheng S, Yang YL, Yang H, Tian SG (2020) Wheat TabZIP8, 9, 13 participate in ABA biosynthesis in NaCl-stressed roots regulated by TaCDPK9-1. Plant Physiol Biochem 151:650–658. https://doi.org/10.1016/j.plaphy.2020.03.039
Zhang Y, Li GY, Si LB, Liu N, Gao TP, Yang YL (2021) Effects of tea polyphenols on the activities of antioxidant enzymes and the expression of related gene in the leaves of wheat seedlings under salt stress. Environ Sci Pollut Res 28:65447–65461. https://doi.org/10.1007/S11356-021-15492-Z
Zhang XH, Ma C, Zhang L, Su M, Wang J, Zheng S, Zhang TG (2022) GR24-mediated enhancement of salt tolerance and roles of H2O2 and Ca2+ in regulating this enhancement in cucumber. J Plant Physiol 270:153640. https://doi.org/10.1016/j.jplph.2022.153640
Zhang XY, He PY, Guo RY, Huang KF, Huang XY (2023) Effects of salt stress on root morphology, carbon and nitrogen metabolism, and yield of Tartary buckwheat. Sci Rep 13:12483. https://doi.org/10.1038/s41598-023-39634-0
Zhu YX, Guo J, Feng R, Jia JH, Han WH, Gong HJ (2016) The regulatory role of silicon on carbohydrate metabolism in Cucumis sativus L. under salt stress. Plant Soil 406:231–249. https://doi.org/10.1007/s11104-016-2877-2
Zhu HY, He MW, Jahan MS, Wu JQ, Gu QS, Shu S, Sun J, Guo SR (2021) CsCDPK6, a CsSAMS1-interacting protein, affects polyamine/ethylene biosynthesis in cucumber and enhances salt tolerance by overexpression in tobacco. Int J Mol Sci 22(20):11133. https://doi.org/10.3390/ijms222011133
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This work was financially supported by the National Natural Science Foundation of China (No. 32160749).
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YZ performed most part of the experiment and analyzed the data. DQ analyzed the data and wrote and edited. ZZ consulted and provided literature. YL and SS worked together with YZ to accomplish partial experiment. YY designed the research and edited the manuscript. In addition, YY was the corresponding author of this manuscript.
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Zhang, Y., Qiao, D., Zhang, Z. et al. Calcium signal regulated carbohydrate metabolism in wheat seedlings under salinity stress. Physiol Mol Biol Plants 30, 123–136 (2024). https://doi.org/10.1007/s12298-024-01413-0
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DOI: https://doi.org/10.1007/s12298-024-01413-0