Silicon alleviates salinity stress in licorice (Glycyrrhiza uralensis) by regulating carbon and nitrogen metabolism

Aslam, M., Ahmad, K., Arslan, A. M. & Amir, M. M. Salinity stress in crop plants: Effects of stress, tolerance mechanisms and breeding strategies for improvement. J. Agric. Basic Sci. 2(1), 2518–4210 (2017).

Google Scholar 

Kirsten, B., Abbey, F. W., Thomas, D., Amitava, C. & Jason, H. Soil salinity: A threat to global food security. Agron. J. 108(6), 2189–2200 (2016).

Article  CAS  Google Scholar 

Shakeel, A. A. et al. Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front. Plant Sci. 8(69), 1–12 (2017).

Google Scholar 

Abd-ElBaki, G. K. et al. Nitrate reductase in Zea mays L. under salinity. Plant Cell Environ. 23, 515–521 (2000).

CAS  Article  Google Scholar 

Flores, P., Botella, M. Á., Martínez, V. & Cerdá, A. C. Ionic and osmotic effects of nitrate reductase activity in tomato seedlings. J. Plant Physiol. 156, 552–557 (2000).

CAS  Article  Google Scholar 

Petronia, C., Gabriella, M., Francesco, N. & Amodio, F. Nitrate reductase in durum wheat seedlings as affected by nitrate nutrition and salinity. Funct. Plant Biol. 32(3), 209–219 (2005).

Article  Google Scholar 

Flowers, T. J. et al. Salt sensitivity in chickpea. Plant Cell Environ. 3(4), 490–509 (2010).

MathSciNet  Article  CAS  Google Scholar 

Husen, A., Iqbal, M., Sohrab, S. S. & Ansari, M. K. A. Salicylic acid alleviates salinity-caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata A. Br.). Agric. Food Secur. 7(1), 44 (2018).

Article  Google Scholar 

Farhangi-Abriz, S. & Torabian, S. Biochar improved nodulation and nitrogen metabolism of soybean under salt stress. Symbiosis. 74(3), 215–223 (2018).

CAS  Article  Google Scholar 

Gupta, B. & Huan, B. Mechanism of salinity tolerance in plants: Physiological, biochemical, and molecular characterization. Int. J. Genomics. 1, 701596. https://doi.org/10.1155/2014/701596 (2014).

CAS  Article  Google Scholar 

Zhang, W. J. et al. Silicon promotes growth and root yield of Glycyrrhiza uralensis, under salt and drought stresses through enhancing osmotic adjustment and regulating antioxidant metabolism. Crop Prot. 107, 1–11 (2018).

Article  CAS  Google Scholar 

Saqib, M., Zörb, C. & Schubert, S. Salt resistant and salt-sensitive wheat genotypes show similar biochemical reaction at protein level in the first phase of salt stress. J. Plant Nutr. Soil Sci. 169(4), 542–548 (2006).

CAS  Article  Google Scholar 

Turan, M. A., Katkat, V. & Taban, S. Salinity-induced stomatal resistance, proline, chlorophyll and ion concentrations of bean. Int. J. Agric. Res. 2(5), 483–488 (2007).

CAS  Article  Google Scholar 

Memon, S. A., Hou, X. L. & Wang, L. J. Morphological analysis of salt stress response of pak Choi. Electron. J. Environ. Agric. Food Chem. 9(1), 248–254 (2010).

CAS  Google Scholar 

Keyvan, A. & Setsuko, K. Crop and medicinal plants proteomics in response to salt stress. Front. Plant Sci. 4(8), 8 (2013).

Google Scholar 

Dadkhah, A. R. Effect of salt stress on growth and essential oil of Matricaria chamomilla. Planta Med. 5(10), 643–646 (2010).

Google Scholar 

Aziz, E. E., Al-Amier, H. & Craker, L. E. Influence of salt stress on growth and essential oil production in peppermint, pennyroyal, and apple mint. J. Herbs Spices Med. Plants. 14(1–2), 77–87 (2008).

CAS  Article  Google Scholar 

Leithy, S., Gaballah, M. S. & Gomaa, A. M. Associative impact of bio-and organic fertilizers on geranium plants grown under saline conditions. Electron. J. Environ. Agric. Food Chem. 1(3), 617–626 (2009).

Google Scholar 

Najafian, S., Khoshkhui, M. & Tavallali, V. Effect of salicylic acid and salinity in rosemary (Rosmarinus officinalis L): Investigation on changes in gas exchange, water relations, and membrane stabilization. Aust. J. Basic. Appl. Sci. 3(3), 322–328 (2009).

CAS  Google Scholar 

Taarit, M. B. et al. Plant growth, essential oil yield and composition of sage (Salvia officinalis L.) fruits cultivated under salt stress conditions. Ind. Crops Prod. 30(3), 333–337 (2009).

Article  CAS  Google Scholar 

Queslati, S. et al. Physiological and antioxidant responses of Mentha pulegium (Pennyroyal) to salt stress. Acta Physiol. Plant. 32(2), 289–296 (2010).

Article  CAS  Google Scholar 

Seyed, M. Z., Faezeh, M., Saadat, S. & Mohsen, P. Selenium and silica nanostructure-based recovery of strawberry plants subjected to drought stress. Sci. Rep. 10, 17672. https://doi.org/10.1038/s41598-020-74273-9 (2020).

CAS  Article  Google Scholar 

Yan, et al. Silicon improves rice salinity resistance by alleviating ionic toxicity and osmotic constraint in an organ-specific pattern. Front. Plant Sci. 11, 260. https://doi.org/10.3389/fpls.2020.00260 (2020).

ADS  Article  PubMed  PubMed Central  Google Scholar 

Mateos-Naranjo, E., Andrades-Moreno, L. & Davy, A. J. Silicon alleviates deleterious effects of high salinity on the halophytic grass Spartina densiflora. Plant Physiol. Biochem. 63, 115–121 (2013).

CAS  PubMed  Article  PubMed Central  Google Scholar 

Chen, D. Q., Yin, L., Deng, X. P. & Wang, S. W. Silicon increases salt tolerance by influencing the two-phase growth response to salinity in wheat (Triticum aestivum L). Acta Physiol. Plant. 36(9), 2531–2535 (2014).

CAS  Article  Google Scholar 

Khattab, H. I., Emam, M. A., Emam, M. M., Helal, N. M. & Mohamed, R. M. Effect of selenium and silicon on transcription factors NAC5 and DREB2A involved in drought-responsive gene expression in rice. Biol. Plant. 58(2), 265–273 (2014).

CAS  Article  Google Scholar 

Zhu, Y. X. & Gong, H. G. Beneficial effects of silicon on salt and drought tolerance in plants. Agron. Sustain. Dev. 34(2), 455–472 (2013).

Article  CAS  Google Scholar 

Zhang, X. H. et al. Effect of silicon on seed germination and the physiological characteristics of Glycyrrhiza uralensis under different levels of salinity. J. Hortic. Sci. Biotechnol. 90(4), 439–443 (2015).

CAS  Article  Google Scholar 

Marcin, R. N. & Maria, S. The relationship between carbon and nitrogen metabolism in cucumber leaves acclimated to salt stress. Peer J. 6(3), e6043 (2018).

Google Scholar 

Zhang, D. D. et al. Enhanced of α-ketoglutarate production in Torulopsis glabrata: Redistribution of carbon flux from pyruvate to α-ketoglutarate. Biotechnol. Bioprocess Eng. 14(2), 134–139 (2009).

ADS  CAS  Article  Google Scholar 

Nunes-Nesi, A., Fernie, A. R. & Stitt, M. Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol. Plant. 3(6), 973–996 (2010).

CAS  PubMed  Article  PubMed Central  Google Scholar 

Miller, A. J., Fan, X. R., Shen, Q. R. & Smith, S. J. Amino acids and nitrate as signals for the regulation of nitrogen acquisition. J. Exp. Bot. 59(1), 111–119 (2008).

CAS  PubMed  Article  PubMed Central  Google Scholar 

Reynolds, M. P. Raising yield potential of wheat. III. Optimizing partitioning to grain while maintaining lodging resistance. J. Exp. Bot. 62(2), 469–486 (2010).

PubMed  PubMed Central  Google Scholar 

Yan, B. B. et al. The effects of endogenous hormones on the flowering and fruiting of Glycyrrhiza uralensis. Plants Basel. 8(11), 519 (2019).

CAS  PubMed Central  Article  Google Scholar 

Mochida, K. et al. Draft genome assembly and annotation of Glycyrrhiza uralensis, a medicinal legume. Plant J. 89(2), 181–194 (2016).

PubMed  Article  CAS  PubMed Central  Google Scholar 

An, C.-G. et al. Effect of KCl or K₂SO₄ supplement to nutrient solution on yield and fruit quality in sweet peppers (Capsicum annuum “Special” and ’Fiesta’). Hortic. Sci. Technol. 24(2), 181–189 (2006).

Google Scholar 

Lang, D. Y., Yu, X. X., Jia, X. X., Li, Z. X. & Zhang, X. H. Methyl jasmonate improves metabolism and growth of NaCl-stressed Glycyrrhiza uralensis seedlings. Sci. Hortic. 266, 109287. https://doi.org/10.1016/j.scienta (2020).

CAS  Article  Google Scholar 

Verma, A. K., Upadhyay, S. K., Verma, P. C., Solomon, S. & Singh, S. B. Functional analysis of sucrose phosphate synthase (SPS) and sucrose synthase (SS) in sugarcane (Saccharum) cultivars. Plant Biol. 13(2), 325–332 (2010).

PubMed  Article  CAS  PubMed Central  Google Scholar 

Orathai, W., Lih, S. K. & Liang, Y. S. The changes in physical, bio-chemical, physiological characteristics and enzyme activities of mango cv. Jinhwang during fruit growth and development. NJAS-Wagen. J. Life Sc. 72–73, 7–12 (2015).

Google Scholar 

Charles, J. B., Christine, H. F., Janice, T., Stephen, A. R. & Quick, W. P. Elevated sucrose-phosphate synthase activity in transgenic tobacco sustains photosynthesis in older leaves and alters development. J. Exp. Bot. 54(389), 1813–1820 (2003).

Article  Google Scholar 

Wang, X. W. et al. In vitro evaluation of the hypoglycemic properties of lactic acid bacteria and its fermentation adaptability in apple juice. LWT-Food Sci. Technol. 136, 110363. https://doi.org/10.1016/j.lwt.2020.110363 (2020).

CAS  Article  Google Scholar 

Ali, A., Jha, P., Sandhu, K. S. & Raghuram, N. Spirulina nitrate-assimilating enzymes (NR, NiR, GS) have higher specific activities and are more stable than those of rice. Physiol. Mol. Biol. Plant. 14(3), 179–182 (2008).

CAS  Article  Google Scholar 

Patel, J. G., Kumar, N. J. I., Kumar, R. N. & Khan, S. R. Evaluation of nitrogen fixing enzyme activities in response to pyrene bioremediation efficacy by defined artificial microalgal-bacterial consortium of Gujarat, India. Polycycl. Aromat. Compd. 38(3), 282–293 (2018).

CAS  Article  Google Scholar 

Liu, C. G. et al. Carbon and nitrogen metabolism in leaves and roots of dwarf bamboo (Fargesia denudata Yi) subjected to drought for two consecutive years during sprouting period. J. Plant Growth Regul. 33, 243–255 (2014).

CAS  Article  Google Scholar 

Magomya, A. M., Kubmarawa, D., Ndahi, J. A. & Yebpella, G. G. Determination of plant proteins via the Kjeldahl method and amino acid analysis: A comparative study. Int. J. Sci. Technol. Res. 3(4), 68–72 (2014).

Google Scholar 

Yang, H. L. et al. Molybdenum blue photometry method for the determination of colloidal silica and soluble silica in leaching solution. Anal. Methods. https://doi.org/10.1039/C5AY01306B (2015).

Article  Google Scholar 

Marino, D., González, E. M. & Arrese-Igor, C. Drought effects on carbon and nitrogen metabolism of pea nodules can be mimicked by paraquat: Evidence for the occurrence of two regulation pathways under oxidative stresses. J. Exp. Bot. 57(3), 665–673 (2006).

CAS  PubMed  Article  PubMed Central  Google Scholar 

Shao, Q. S. et al. Effects of NaCl stress on nitrogen metabolism of cucumber seedlings. Russ. J. Plant Physiol. 62(5), 595–603 (2015).

CAS  Article  Google Scholar 

Irani, S. & Todd, C. D. Ureide metabolism under abiotic stress in Arabidopsis thaliana. J. Plant Physiol. 199, 87–95 (2016).

CAS  PubMed  Article  PubMed Central  Google Scholar 

Ahmad, P. et al. Silicon (Si) supplementation alleviates NaCl toxicity in Mung Bean [Vigna radiata, (L.) Wilczek] through the modifications of physio-biochemical attributes and key antioxidant enzymes. J. Plant Growth Regul. 38, 70–82 (2018).

Article  CAS  Google Scholar 

Liang, Y. C., Chen, Q., Liu, Q., Zhang, W. H. & Ding, R. X. Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). J. Plant Physiol. 160(10), 1157–1164 (2003).

CAS  PubMed  Article  PubMed Central  Google Scholar 

Kim, Y. H. et al. Silicon application to rice root zone influenced the phytohormonal and antioxidant responses under salinity stress. J. Plant Growth Regul. 33(2), 137–149 (2013).

Article  CAS  Google Scholar 

Haghighi, M. & Pessarakli, M. Influence of silicon and nano-silicon on salinity tolerance of cherry tomatoes (Solanum lycopersicum L.) at early growth stage. Sci. Hortic. 161(24), 111–117 (2013).

CAS  Article  Google Scholar 

Zhu, Y. X. et al. Silicon improves salt tolerance by increasing root water uptake in Cucumis sativus, L. Plant Cell Rep. 34(9), 1629–1646 (2015).

CAS  PubMed  Article  PubMed Central  Google Scholar 

Fernandes, F. M., Arrabaca, M. C. & Carvalho, L. M. M. Sucrose metabolism in Lupinus albus L. under salt stress. Biol. Plant. 48(2), 317–319 (2004).

CAS  Article  Google Scholar 

Miyako, K. et al. Cytosolic GLUTAMINE SYNTHETASE1;1 modulates metabolism and chloroplast development in roots. Plant Physiol. 182(4), 1894–1909 (2020).

Article  CAS  Google Scholar 

Joaquim, A. G. S. et al. Proline accumulation and glutamine synthetase activity are increased by salt-induced proteolysis in cashew leaves. J. Plant Physiol. 160(2), 115–123 (2003).

Article  Google Scholar 

Dresler, S., Wójcik, M., Bednarek, W., Hanaka, A. & Tukiendorf, A. The effect of silicon on maize growth under cadmium stress. Russ. J. Plant Physiol. 62(1), 86–92 (2015).

CAS  Article  Google Scholar 

Muneer, S. & Jeong, B. R. Proteomic analysis of salt-stress responsive proteins in roots of tomato (Lycopersicon esculentum L.) plants towards silicon efficiency. Plant Growth Regul. 77(2), 133–146 (2015).

ADS  CAS  Article  Google Scholar 

Dorairaj, D., Ismail, M. R., Sinniah, U. R. & Ban, T. K. Influence of silicon on growth, yield, and lodging resistance of MR219, a lowland rice of Malaysia. J. Plant Nutr. 40(8), 1111–1124 (2017).

CAS  Article  Google Scholar 

Garg, N. & Singh, S. Arbuscular mycorrhiza Rhizophagus irregularis and silicon modulate growth, proline biosynthesis and yield in Cajanus cajan L. Millsp. (pigeonpea) genotypes under cadmium and zinc stress. J. Plant Growth Regul. 37(6), 46–63 (2018).

CAS  Article  Google Scholar