Exogenous zinc application mitigates negative effects of salinity on barley (Hordeum vulgare) growth by improving root ionic homeostasis

Waleed Amjad Khan; Beth Penrose; Ping Yun; Meixue Zhou; Sergey Shabala

doi:10.1071/FP23266

RESEARCH ARTICLE (Open Access)

Previous Next Contents Vol 51(6)

Exogenous zinc application mitigates negative effects of salinity on barley (Hordeum vulgare) growth by improving root ionic homeostasis

Waleed Amjad Khan ^A , Beth Penrose ^A , Ping Yun ^A , Meixue Zhou

^A and Sergey Shabala

^A ^B ^C ^*

+ Author Affiliations

- Author Affiliations

^A Tasmanian Institute of Agriculture, University of Tasmania, Hobart, Tas. 7001, Australia.

^B International Research Centre for Environmental Membrane Biology, Foshan University, Foshan 528000, China.

^C School of Biological Science, University of Western Australia, Crawley, WA 6009, Australia.

^* Correspondence to: Sergey.Shabala@uwa.edu.au

Handling Editor: Vadim Demidchik

Functional Plant Biology 51, FP23266 https://doi.org/10.1071/FP23266

Submitted: 8 November 2023 Accepted: 25 April 2024 Published: 16 May 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Detrimental effects of salinity could be mitigated by exogenous zinc (Zn) application; however, the mechanisms underlying this amelioration are poorly understood. This study demonstrated the interaction between Zn and salinity by measuring plant biomass, photosynthetic performance, ion concentrations, ROS accumulation, antioxidant activity and electrophysiological parameters in barley (Hordeum vulgare L.). Salinity stress (200 mM NaCl for 3 weeks) resulted in a massive reduction in plant biomass; however, both fresh and dry weight of shoots were increased by ~30% with adequate Zn supply. Zinc supplementation also maintained K⁺ and Na⁺ homeostasis and prevented H₂O₂ toxicity under salinity stress. Furthermore, exposure to 10 mM H₂O₂ resulted in massive K⁺ efflux from root epidermal cells in both the elongation and mature root zones, and pre-treating roots with Zn reduced ROS-induced K⁺ efflux from the roots by 3–4-fold. Similar results were observed for Ca²⁺. The observed effects may be causally related to more efficient regulation of cation-permeable non-selective channels involved in the transport and sequestration of Na⁺, K⁺ and Ca²⁺ in various cellular compartments and tissues. This study provides valuable insights into Zn protective functions in plants and encourages the use of Zn fertilisers in barley crops grown on salt-affected soils.

Keywords: antioxidant activity, barley, calcium, non-selective cation channels, potassium, reactive oxygen species, root epidermis, sodium.

References

AbdElgawad H, Zinta G, Hegab MM, Pandey R, Asard H, Abuelsoud W (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Frontiers in Plant Science 7, 276.
| Crossref | Google Scholar |

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121-126.
| Google Scholar | PubMed |

Agarwal P, Khurana P (2018) Characterization of a novel zinc finger transcription factor (TaZnF) from wheat conferring heat stress tolerance in Arabidopsis. Cell Stress and Chaperones 23(2), 253-267.
| Crossref | Google Scholar |

Anwar S, Khalilzadeh R, Khan S, Zaib un N, Bashir R, Pirzad A, Malik A (2021) Mitigation of drought stress and yield improvement in wheat by zinc foliar spray relates to enhanced water use efficiency and zinc contents. International Journal of Plant Production 15(3), 377-389.
| Crossref | Google Scholar |

Begum F, Haque MA, Alam MS, Mohanta HC (2015) Evaluation of sweet potato genotypes against salinity. Bangladesh Journal of Agricultural Research 40, 249-257.
| Crossref | Google Scholar |

Bojórquez-Quintal E, Velarde-Buendía A, Ku-González Á, Carillo-Pech M, Ortega-Camacho D, Echevarría-Machado I, Pottosin I, Martínez-Estévez M (2014) Mechanisms of salt tolerance in habanero pepper plants (Capsicum chinense Jacq.): proline accumulation, ions dynamics and sodium root-shoot partition and compartmentation. Frontiers in Plant Science 5, 605.
| Crossref | Google Scholar |

Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2014) Rapid regulation of the plasma membrane H⁺-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Annals of Botany 115(3), 481-494.
| Crossref | Google Scholar |

Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytologist 173, 677-702.
| Crossref | Google Scholar | PubMed |

Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na⁺ exclusion loci in wheat, Nax2 and Kna1. Plant Physiology 143(4), 1918-1928.
| Crossref | Google Scholar |

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 & Environment 28, 1230-1246.
| Crossref | Google Scholar |

Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. Journal of Experimental Botany 58, 4245-4255.
| Crossref | Google Scholar | PubMed |

Chen Z, Xie Y, Gu Q, Zhao G, Zhang Y, Cui W, Xu S, Wang R, Shen W (2017) The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radical Biology and Medicine 108, 465-477.
| Crossref | Google Scholar | PubMed |

Colmenero-Flores JM, Martínez G, Gamba G, Vázquez N, Iglesias DJ, Brumós J, Talón M (2007) Identification and functional characterization of cation–chloride cotransporters in plants. The Plant Journal 50(2), 278-292.
| Crossref | Google Scholar |

Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K⁺ correlates with salt tolerance in wheat. Journal of Experimental Botany 59, 2697-2706.
| Crossref | Google Scholar | PubMed |

Cuin TA, Tian Y, Betts SA, Chalmandrier R, Shabala S (2009) Ionic relations and osmotic adjustment in durum and bread wheat under saline conditions. Functional Plant Biology 36, 1110-1119.
| Crossref | Google Scholar |

Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environmental and Experimental Botany 109, 212-228.
| Crossref | Google Scholar |

Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 175(3), 387-404.
| Crossref | Google Scholar |

Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiology 128, 379-387.
| Crossref | Google Scholar |

Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca²⁺- and K⁺-permeable channels in plant root cells. Journal of Cell Science 116(1), 81-88.
| Crossref | Google Scholar |

Demidchik V, Shabala SN, Davies JM (2007) Spatial variation in H₂O₂ response of Arabidopsis thaliana root epidermal Ca²⁺ flux and plasma membrane Ca²⁺ channels. The Plant Journal 49(3), 377-386.
| Crossref | Google Scholar |

Demidchik V, Shabala S, Isayenkov S, Cuin TA, Pottosin I (2018) Calcium transport across plant membranes: mechanisms and functions. New Phytologist 220, 49-69.
| Crossref | Google Scholar | PubMed |

Dreyer BH, Schippers JHM (2019) Copper-zinc superoxide dismutases in plants: evolution, enzymatic properties, and beyond. In ‘Annual plant reviews online. Vol. 2(3)’. (Ed. JA Roberts) pp. 1–36. (American Cancer Society) doi:10.1002/9781119312994.apr0705

Guo P, Wei H, Zhang W, Bao Y (2016) Physiological responses of alfalfa to high-level salt stress: root ion flux and stomatal characteristics. International Journal of Agriculture and Biology 18, 125-133.
| Google Scholar |

Habashy WS, Milfort MC, Rekaya R, Aggrey SE (2019) Cellular antioxidant enzyme activity and biomarkers for oxidative stress are affected by heat stress. International Journal of Biometeorology 63, 1569-1584.
| Crossref | Google Scholar | PubMed |

Han G, Lu C, Guo J, Qiao Z, Sui N, Qiu N, Wang B (2020) C2H2 zinc finger proteins: master regulators of abiotic stress responses in plants. Frontiers in Plant Science 11, 115.
| Crossref | Google Scholar |

Han G, Qiao Z, Li Y, Yang Z, Wang C, Zhang Y, Liu L, Wang B (2022) RING zinc finger proteins in plant abiotic stress tolerance. Frontiers in Plant Science 13, 877011.
| Crossref | Google Scholar |

Hara T, Takeda T-A, Takagishi T, Fukue K, Kambe T, Fukada T (2017) Physiological roles of zinc transporters: molecular and genetic importance in zinc homeostasis. The Journal of Physiological Sciences 67, 283-301.
| Crossref | Google Scholar |

Hedrich R, Shabala S (2018) Stomata in a saline world. Current Opinion in Plant Biology 46, 87-95.
| Crossref | Google Scholar |

Hussein MM, Alva AK (2014) Effects of zinc and ascorbic acid application on the growth and photosynthetic pigments of millet plants grown under different salinity. Agricultural Sciences 5, 1253-1260.
| Crossref | Google Scholar |

Iqbal MN, Rasheed R, Ashraf MY, Ashraf MA, Hussain I (2018) Exogenously applied zinc and copper mitigate salinity effect in maize (Zea mays L.) by improving key physiological and biochemical attributes. Environmental Science and Pollution Research 25(24), 23883-23896.
| Crossref | Google Scholar |

Ireland SM, Martin ACR (2019) ZincBind—the database of zinc binding sites. Database 2019 baz006.
| Crossref | Google Scholar |

Jan AU, Hadi F, Midrarullah , Nawaz MA, Rahman K (2017) Potassium and zinc increase tolerance to salt stress in wheat (Triticum aestivum L.). Plant Physiology and Biochemistry 116, 139-149.
| Crossref | Google Scholar | PubMed |

Khan AR, Wakeel A, Muhammad N, Liu B, Wu M, Liu Y, Ali I, Zaidi SHR, Azhar W, Song G (2019) Involvement of ethylene signaling in zinc oxide nanoparticle-mediated biochemical changes in Arabidopsis thaliana leaves. Environmental Science: Nano 6, 341-355.
| Google Scholar |

Li Z, Han X, Song X, Zhang Y, Jiang J, Han Q, Liu M, Qiao G, Zhuo R (2017) Overexpressing the Sedum alfredii Cu/Zn superoxide dismutase increased resistance to oxidative stress in transgenic Arabidopsis. Frontiers in Plant Science 8, 1010.
| Crossref | Google Scholar |

Liu X, Li R, Dai Y, Yuan L, Sun Q, Zhang S, Wang X (2019) A B-box zinc finger protein, MdBBX10, enhanced salt and drought stresses tolerance in Arabidopsis. Plant Molecular Biology 99, 437-447.
| Crossref | Google Scholar | PubMed |

Luo X, Dai Y, Zheng C, Yang Y, Chen W, Wang Q, Chandrasekaran U, Du J, Liu W, Shu K (2021) The ABI4-RbohD/VTC2 regulatory module promotes reactive oxygen species (ROS) accumulation to decrease seed germination under salinity stress. New Phytologist 229, 950-962.
| Crossref | Google Scholar | PubMed |

Maksimović JD, Zhang J, Zeng F, Živanović BD, Shabala L, Zhou M, Shabala S (2013) Linking oxidative and salinity stress tolerance in barley: can root antioxidant enzyme activity be used as a measure of stress tolerance? Plant and Soil 365, 141-155.
| Crossref | Google Scholar |

Mori A, Kirk GJD, Lee J-S, Morete MJ, Nanda AK, Johnson-Beebout SE, Wissuwa M (2016) Rice genotype differences in tolerance of zinc-deficient soils: evidence for the importance of root-induced changes in the rhizosphere. Frontiers in Plant Science 6, 1160.
| Crossref | Google Scholar |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25(2), 239-250.
| Crossref | Google Scholar |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651-681 [In eng].
| Crossref | Google Scholar |

Natasha N, Shahid M, Bibi I, Iqbal J, Khalid S, Murtaza B, Bakhat HF, Farooq ABU, Amjad M, Hammad HM, Niazi NK, Arshad M (2022) Zinc in soil-plant-human system: a data-analysis review. Science of The Total Environment 808, 152024.
| Crossref | Google Scholar |

Pan T, Liu M, Kreslavski VD, Zharmukhamedov SK, Nie C, Yu M, Kuznetsov VV, Allakhverdiev SI, Shabala S (2021) Non-stomatal limitation of photosynthesis by soil salinity. Critical Reviews in Environmental Science and Technology 51(8), 791-825.
| Crossref | Google Scholar |

Pandolfi C, Pottosin I, Cuin T, Mancuso S, Shabala S (2010) Specificity of polyamine effects on NaCl-induced ion flux kinetics and salt stress amelioration in plants. Plant and Cell Physiology 51, 422-434.
| Crossref | Google Scholar | PubMed |

Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731-734.
| Google Scholar |

Percey WJ, McMinn A, Bose J, Breadmore MC, Guijt RM, Shabala S (2016) Salinity effects on chloroplast PSII performance in glycophytes and halophytes. Functional Plant Biology 43, 1003-1015.
| Crossref | Google Scholar | PubMed |

Redwan M, Spinelli F, Marti L, Weiland M, Palm E, Azzarello E, Mancuso S (2016) Potassium fluxes and reactive oxygen species production as potential indicators of salt tolerance in Cucumis sativus. Functional Plant Biology 43, 1016-1027.
| Crossref | Google Scholar | PubMed |

Robson A (2012) Zinc in soils and plants. In ‘Proceedings of the international symposium on ‘zinc in soils and plants’ held at the University of Western Australia, 27–28 September, 1993’. (Springer: Dordrecht, Netherlands)

Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Current Opinion in Biotechnology 26, 115-124.
| Crossref | Google Scholar | PubMed |

Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675.
| Crossref | Google Scholar | PubMed |

Senthilkumar M, Amaresan N, Sankaranarayanan A (2021) Estimation of superoxide dismutase (SOD). In ‘Plant-microbe interactions: laboratory techniques.’ (Eds M Senthilkumar, N Amaresan, A Sankaranarayanan) pp. 117–118. (Springer: New York, NY, USA)

Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Annals of Botany 112(7), 1209-1221.
| Crossref | Google Scholar |

Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiologia Plantarum 151, 257-279.
| Crossref | Google Scholar | PubMed |

Shabala SN, Newman IA, Morris J (1997) Oscillations in H⁺ and Ca²⁺ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiology 113, 111-118.
| Crossref | Google Scholar | PubMed |

Shabala L, Cuin TA, Newman IA, Shabala S (2005) Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 222(6), 1041-1050.
| Crossref | Google Scholar |

Shabala L, Ross T, McMeekin T, Shabala S (2006) Non-invasive microelectrode ion flux measurements to study adaptive responses of microorganisms to the environment. FEMS Microbiology Reviews 30, 472-486.
| Crossref | Google Scholar | PubMed |

Shabala S, Bose J, Fuglsang AT, Pottosin I (2016) On a quest for stress tolerance genes: Membrane transporters in sensing and adapting to hostile soils. Journal of Experimental Botany 67, 1015-1031.
| Crossref | Google Scholar | PubMed |

Shahid SA, Zaman M, Heng L (2018) Soil salinity: historical perspectives and a world overview of the problem. In ‘Guideline for salinity assessment, mitigation and adaptation using nuclear and related techniques’. (Eds M Zaman, SA Shahid, L Heng) pp. 43–53. (Springer International Publishing: Cham, Switzerland)

Shahzad B, Yun P, Rasouli F, Shabala L, Zhou M, Venkataraman G, Chen Z-H, Shabala S (2022) Root K⁺ homeostasis and signalling as a determinant of salinity stress tolerance in cultivated and wild rice species. Environmental and Experimental Botany 201, 104944.
| Crossref | Google Scholar |

Shi H, Ishitani M, Kim C, Zhu J-K (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na⁺/H⁺ antiporter. Proceedings of the National Academy of Sciences 97(12), 6896-6901.
| Crossref | Google Scholar |

Smethurst CF, Rix K, Garnett T, Auricht G, Bayart A, Lane P, Wilson SJ, Shabala S (2008) Multiple traits associated with salt tolerance in lucerne: revealing the underlying cellular mechanisms. Functional Plant Biology 35, 640-650.
| Crossref | Google Scholar | PubMed |

Stanton C, Sanders D, Krämer U, Podar D (2022) Zinc in plants: integrating homeostasis and biofortification. Molecular Plant 15, 65-85.
| Crossref | Google Scholar | PubMed |

Sun Y, Kong X, Li C, Liu Y, Ding Z (2015) Potassium retention under salt stress is associated with natural variation in salinity tolerance among Arabidopsis accessions. PLoS ONE 10, e0124032.
| Crossref | Google Scholar | PubMed |

Tavallali V, Rahemi M, Maftoun M, Panahi B, Karimi S, Ramezanian A, Vaezpour M (2009) Zinc influence and salt stress on photosynthesis, water relations, and carbonic anhydrase activity in pistachio. Scientia Horticulturae 123, 272-279.
| Google Scholar |

Tavallali V, Rahemi M, Eshghi SRT, Kholdebarin B, Ramezanian A (2010) Zinc alleviates salt stress and increases antioxidant enzyme activity in the leaves of pistachio (Pistacia vera L. ‘Badami’) seedlings. Turkish Journal of Agriculture and Forestry 34, 349-359.
| Google Scholar |

Tolay I (2021) The impact of different zinc (Zn) levels on growth and nutrient uptake of Basil (Ocimum basilicum L.) grown under salinity stress. PLoS ONE 16, e0246493.
| Crossref | Google Scholar | PubMed |

Tufail A, Li H, Naeem A, Li TX (2018) Leaf cell membrane stability-based mechanisms of zinc nutrition in mitigating salinity stress in rice. Plant Biology 20(2), 338-345.
| Crossref | Google Scholar |

Turan S, Tripathy BC (2015) Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiologia Plantarum 153(3), 477-491.
| Crossref | Google Scholar |

van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annual Review of Plant Biology 71, 403-433.
| Crossref | Google Scholar |

Velarde-Buendía AM, Shabala S, Cvikrova M, Dobrovinskaya O, Pottosin I (2012) Salt-sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K⁺ efflux by polyamines. Plant Physiology and Biochemistry 61, 18-23.
| Crossref | Google Scholar |

Wang N, Qi H, Su G, Yang J, Zhou H, Xu Q, Huang Q, Yan G (2016) Genotypic variations in ion homeostasis, photochemical efficiency and antioxidant capacity adjustment to salinity in cotton (Gossypium hirsutum L.). Soil Science and Plant Nutrition 62, 240-246.
| Crossref | Google Scholar |

Wang H, Shabala L, Zhou M, Shabala S (2018) Hydrogen peroxide-induced root Ca²⁺ and K⁺ fluxes correlate with salt tolerance in cereals: towards the cell-based phenotyping. International Journal of Molecular Sciences 19, 702.
| Crossref | Google Scholar | PubMed |

Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Badakhshan H (2014) Effects of zinc application on growth, absorption and distribution of mineral nutrients under salinity stress in soybean (Glycine Max L.). Journal of Plant Nutrition 37(14), 2255-2269.
| Crossref | Google Scholar |

Wu H, Shabala L, Shabala S, Giraldo JP (2018) Hydroxyl radical scavenging by cerium oxide nanoparticles improves Arabidopsis salinity tolerance by enhancing leaf mesophyll potassium retention. Environmental Science: Nano 5, 1567-1583.
| Crossref | Google Scholar |

Zafar Z, Rasheed F, Haq AU, Ibrahim FH, Afzal S, Nazre M, Akram S, Hussain Z, Kudus KA, Mohsin M, Qadeer A, Raza Z, Khan WR (2021) Interspecific differences in physiological and biochemical traits drive the water stress tolerance in young Morus alba L. and Conocarpus erectus L. saplings. Plants 10, 1615 10.3390/plants10081615.
| Google Scholar |

Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R, Bose J, Shabala S, Muñiz-Murguía J, Pottosin II (2011) Polyamines interact with hydroxyl radicals in activating Ca²⁺ and K⁺ transport across the root epidermal plasma membranes. Plant Physiology 157(4), 2167-2180.
| Crossref | Google Scholar |

Zhang J, Wang S, Song S, Xu F, Pan Y, Wang H (2019) Transcriptomic and proteomic analyses reveal new insight into chlorophyll synthesis and chloroplast structure of maize leaves under zinc deficiency stress. Journal of Proteomics 199, 123-134.
| Crossref | Google Scholar | PubMed |

Zhao C, Zhang H, Song C, Zhu J-K, Shabala S (2020) Mechanisms of plant responses and adaptation to soil salinity. The Innovation 1, 100017.
| Crossref | Google Scholar | PubMed |

Zhu M, Zhou M, Shabala L, Shabala S (2017) Physiological and molecular mechanisms mediating xylem Na⁺ loading in barley in the context of salinity stress tolerance. Plant, Cell & Environment 40(7), 1009-1020.
| Crossref | Google Scholar |