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The mechanism of hydrogen sulfide mitigation of iron deficiency-induced chlorosis in strawberry (Fragaria × ananassa) plants

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Abstract

A study was carried out to assess the mitigation mechanism of exogenously applied sodium hydrosulfide (NaHS) as a donor of H2S on strawberry seedlings under iron deficiency. The ameliorative effects of NaHS on oxidative damage, ion hemostasis and uptake, and availability of Fe were investigated by spraying solution of 0.2 mM NaHS or 0.2 mM NaHS plus 0.2 mM hypotaurine (HT), a scavenger of H2S to plant leaves. Iron deficiency was created using 0.1 mM FeSO4 instead of 0.1 mM EDTA-Fe in Hoagland’s nutrient solution. After a 28-day treatment, strawberry plants exhibited leaf interveinal chlorosis under Fe deficiency, but these apparent symptoms of iron deficiency were overcome by foliar application of NaHS. Exogenously applied NaHS enhanced chlorophyll contents and available iron and Fe accumulation in young leaves, but application of H2S scavenger hypotaurine with NaHS did not change those parameters under Fe deficiency. This clearly shows that NaHS improved iron availability in the strawberry plants. Furthermore, exogenously applied NaHS increased endogenous H2S and iron levels in the roots and leaves. Moreover, NaHS enhanced the levels of zinc (Zn2+), calcium (Ca2+), and magnesium (Mg2+) in both leaves and roots of the strawberry plants grown at Fe deficiency, except for Zn in roots which decreased significantly. This also suggests that NaHS maintains the levels of inorganic ions restricted by Fe deficiency. Fe deficiency increased electrolyte leakage (EL) and the levels of malondialdehyde (MDA) and hydrogen peroxide (H2O2) in plant leaves. Exogenous NaHS reduced the accumulation of H2O2, MDA, and EL and upregulated the activities of key antioxidant enzymes. Overall, NaHS improved Fe uptake and activation by improving endogenous H2S, maintained balance of mineral nutrients and activities of the antioxidant enzymes, and reduced the generation of MDA and H2O2 as well as electrolyte leakage caused by Fe deficiency. So NaHS proved to be effective in ameliorating iron chlorosis caused by iron deficiency.

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References

  • Abdul Jaleel C, Manivannan P, Sankar B, Kishorekumar A, Panneerselvam R (2007) Calcium chloride effects on salinity-induced oxidative stress, proline metabolism and indole alkaloid accumulation in Catharan thusroseus. C R Biol 330:674–683

    Article  CAS  Google Scholar 

  • Alam S, Kamei S, Kawai S (2001) Effect of iron deficiency on the chemical composition of the xylem sap of barley. Soil Sci Plant Nutr 47:643–649

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and assays applicable toacrylamide gels. Anal Biochem 44:276–287

  • Borah KD, Bhuyan J (2017) Magnesium porphyrins with relevance to chlorophylls. Dalton Trans 46:6497–6509

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Briat JF, Dubos C, Gaymard F (2015) Iron nutrition biomass production and plant product quality. Trends Plant Sci 20:33–40

    Article  PubMed  CAS  Google Scholar 

  • Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists Rockville MD ISBN978-0-943088-39-6

  • Bush DS 1993 Regulation of cytosolic calcium in plants. Plant Physiol 1037–13

  • Celik H, Katkat AV (2007) Some parameters in relation to iron nutrition status of peach orchards. J Biol Environ Sci 1:111–115

    Google Scholar 

  • Chance B, Maehly C (1955) Assay of catalase and peroxidases. Methods Enzymol 2:764–775

    Article  Google Scholar 

  • Chapman HD, Pratt PF (1982) Methods of plant analysis I methods of analysis for soils plants and water. Chapman Publishers, Riverside California

    Google Scholar 

  • Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zhen HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis photosynthetic enzyme expression and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He JX, Zheng HL (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318

    Article  CAS  Google Scholar 

  • Chen J, Wu FH, Shang YT, Wang WH, Hu WJ, Simon M, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulphide improves adaptation of Zea mays seedlings to iron deficiency. J Exp Bot 66:6605–6622

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen J, Shang YT, Zhang NN, Zhong YQW, Wang WH, Zhang JH, Shangguan ZP (2018) Sodium hydrosulfide modifies the nutrient ratios of soybean (Glycine max) under iron deficiency. J Plant Nutr Soil Sci 181:305–315

    Article  CAS  Google Scholar 

  • Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defense pathways. J Exp Bot 64:1953–1966

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ding F, Wang XF, Shi QH, Wang ML, Yang FJ, Gao QH (2008) Exogenous nitric oxide alleviated the inhibition of photosynthesis and antioxidant enzyme activities in iron-deficient Chinese cabbage (Brassica chinensis L). Agric Sci China 7:168–179

    Article  CAS  Google Scholar 

  • Ding H, Duan L, Wu H, Yang R, Ling H, Li WX, Zhang F (2009) Regulation of AhFRO1 an Fe (III)-chelate reductase of peanut during iron deficiency stress and intercropping with maize. Physiol Plant 136:274–283

    Article  PubMed  CAS  Google Scholar 

  • Ding H, Duan LH, Li F, Yan HF, Zhao M, Zhang FS, Li WX (2010) Cloning and functional analysis of the peanut iron transporter AhIRT1 during iron deficiency stress and intercropping with maize. J Plant Physiol 167:996–1002

    Article  PubMed  CAS  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  CAS  Google Scholar 

  • Fasaei RG, Ronaghi A (2008) Interaction of iron with copper zinc and manganese in wheat as affected by iron and manganese in calcareous soil. J Plant Nutr 31:839–848

    Article  CAS  Google Scholar 

  • Gao L, Shi YX (2007) Genetic differences in resistance to iron deficiency chlorosis in peanut. J Plant Nutr 30:37–52

    Article  CAS  Google Scholar 

  • Graziano M, Lamattina L (2005) Nitric oxide and iron in plants: an emerging and converging story. Trends Plant Sci 10:4–8

    Article  PubMed  CAS  Google Scholar 

  • Graziano M, Lamattina L (2007) Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J 52:949–960

    Article  PubMed  CAS  Google Scholar 

  • Graziano M, Beligni MV, Lamattina L (2002) Nitric oxide improves internal iron availability in plants. Plant Physiol 130:1852–1859

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147:743–749

    Article  PubMed  CAS  Google Scholar 

  • Guo HM, Zhou H, Zhang J, Guan WX, Xu S, Shen WB, Xu GH, Xie YJ, Foyer CH (2017) L-cysteine desulfhydrase-related H2S production is involved in OsSE5-promoted ammonium tolerance in roots of Oryza sativa. Plant Cell Envir 40:1777–1790

    Article  CAS  Google Scholar 

  • Hällgren JE, Fredriksson SÅ (1982) Emission of hydrogen sulfide from sulfate dioxide-fumigated pine trees. Plant Physiol 70:456–459

    Article  PubMed  PubMed Central  Google Scholar 

  • Herschbach C, van der Zalm E, Scneide A, Jouanin L, De Kok LJ, Rennenberg H (2000) Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing g-glutamyl cysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiol 124:461–473

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jin CW, He XY, Wu P, Zheng SJ (2006) Mechanisms of microbially enhanced Fe acquisition in red clover (Trifolium pretense L). Plant Cell Environ 29:888–897

    Article  PubMed  Google Scholar 

  • Jin CW, You GY, He YF, Tang CX, Wu P, Zheng SJ (2007) Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol 144:278–285

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jin CW, Du ST, Chen WW, Li GX, Zhang YS, Zhang SJ (2009) Elevated carbon dioxide improves plant iron nutrition through enhancing the iron-deficiency-induced responses under iron-limited conditions in tomato. Plant Physiol 150:272–280

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jin CW, Liu Y, Mao QQ, Wang Q, Du ST (2013) Mild Fe-deficiency improves biomass production and quality of hydroponic-cultivated spinach plants (Spinacia oleracea L). Food Chem 138:2188–2194

    Article  PubMed  CAS  Google Scholar 

  • Jin J, Cui H, Lv X, Yang Y, Wang Y, Lu X (2017) Exogenous CaCl2 reduces salt stress in sour jujube by reducing Na+ and increasing K+ Ca2+ and Mg2+ in different plant organs. J Hortic Sci Biotechnol 92:98–106

    Article  CAS  Google Scholar 

  • Kaya C, Ashraf M, Akram NA (2018) Hydrogen sulfide regulates the levels of key metabolites and antioxidant defense system to counteract oxidative stress in pepper (Capsicum annuum L.) plants exposed to high zinc regime. Environ Sci Pollut Res 25:12612–12618

    Article  CAS  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake translocation and regulation in higher plants. Annu Rev Plant Biol 63:131–152

    Article  PubMed  CAS  Google Scholar 

  • Kong J, Dong Y, Xu L, Liu S, Bai X (2014) Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L. Bot Stud 55:9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kraus TE, Fletcher RA (1994) Paclobutrazol protects wheat seedlings from heat and paraquat injury is detoxification of active oxygen involved? Plant Cell Physiol 35:45–52

    CAS  Google Scholar 

  • Lefer DJ (2007) A new gaseous signaling molecule emerges: cardio protective role of hydrogen sulfide. Proc Natl Acad Sci U S A 104:17907–17908

    Article  PubMed  PubMed Central  Google Scholar 

  • Li WF, Lan P (2017) The understanding of the plant iron deficiency responses in strategy i plants and the roleof ethylene in this process by omic approaches. Front Plant Sci 8:40

    PubMed  PubMed Central  Google Scholar 

  • Li D, Xiao Z, Liu L, Wang J, Song G, Bi Y (2010) Effects of exogenous hydrogen sulfide (H2S) on the root tip and root border cells of Pisum sativum. Chin Bull Bot 45:354–362

    CAS  Google Scholar 

  • Li J, Jia H, Wang J, Cao Q, Wen Z (2014) Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na1/H1 antiporter system in the hydrogen peroxide-dependent manner in salt stress Arabidopsis thaliana root. Protoplasma 251:899–912

    Article  PubMed  CAS  Google Scholar 

  • Lin G, Sternberg L (1992) Effect of growth form salinity nutrient and sulfide on photosynthesis carbon isotope discrimination and growth of red mangrove (Rhizophora mangle L). Funct Plant Biol 19:509–517

    Article  CAS  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage quenches ozone products and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2006) Abiotic stress the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  PubMed  CAS  Google Scholar 

  • Molassiotis A, Therios I, Dimassi K, Diamantidis G, Chatzissavvidis C (2005) Induction of Fe (III)-chelate reductase activity by ethylene and salicylic acid in iron-deficient peach rootstock explants. J Plant Nutr 28:669–682

    Article  CAS  Google Scholar 

  • Morales F, Belkhodja R, Abadía A, Abadía J (2000) Photosystem II efficiency and mechanisms of energy dissipation in iron-deficient field-grown pear trees (Pyrus communis L). Photosynth Res 63:9–21

    Article  PubMed  CAS  Google Scholar 

  • Mostofa MG, Saegusa D, Fujita M, Tran LS (2015) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front Plant Sci 6:1055

    Article  PubMed  PubMed Central  Google Scholar 

  • Oren A, Padan E, Malkin S (1979) Sulfide inhibition of photosystem II in cyanobacteria (blue-green algae) and tobacco chloroplasts. Biochem Biophys Acta 546:270–279

    PubMed  CAS  Google Scholar 

  • Pestana M, Correia PJ, Saavedra T, Gama F, Abadía A, de Varennes A (2012) Development and recovery of iron deficiency by iron resupply to roots or leaves of strawberry plants. Plant Physiol Biochem 53:1–5

    Article  PubMed  CAS  Google Scholar 

  • Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084

    Article  PubMed  CAS  Google Scholar 

  • Schmidt W (1999) Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol 141:1–26

    Article  CAS  Google Scholar 

  • Sekiya J, Schmidt A, Wilson LG, Filner P (1982) Emission of hydrogen sulfide by leaf tissue in response to L-cysteine. Plant Physiol 70:430–436

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shi QH, Zhu ZJ (2008) Effects of exogenous salicylic acid on manganese toxicity element contents and antioxidative system in cucumber. Environ Exp Bot 63:317–326

    Article  CAS  Google Scholar 

  • Shi GR, Cai QS, Liu QQ, Wu L (2009) Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake photosynthesis and antioxidant enzymes. Acta Physio Plant 31:969–977

    Article  CAS  Google Scholar 

  • Strain HH, Svec WA (1966) Extraction separation estimation and isolation of the chlorophylls in: Vernon LP Seely GR (Eds) The Chlorophylls Academic Press New York, pp 21–65

  • Takahashi M, Nakanishi H, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19:466–469

    Article  PubMed  CAS  Google Scholar 

  • Van Breusegem F, Varanova E, Dat JF, Inze D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414

    Article  Google Scholar 

  • Wang R (2002) Two’s company three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798

    Article  PubMed  CAS  Google Scholar 

  • Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2012) Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L). Plant Omics J 5:60–67

    CAS  Google Scholar 

  • Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates the oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009) Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250

    Article  CAS  Google Scholar 

  • Zhang XW, Zhang M, Wang QH, Qiu XK, Hu GQ, Dong YJ (2011) Effect of exogenous nitric oxide on physiological characteristic of peanut under iron-deficient stress. J Plant Nutr Fert 17:665–673

    CAS  Google Scholar 

  • Zhang X, Dong Y, Kong J, LiuZ WQ (2014) Effects of nıtrıc oxıde on ıron-defıcıency stress allevıatıon of peanut. J Plant Nutri 37:2108–2127

    Article  CAS  Google Scholar 

  • Zhu CQ, Zhang JH, Sun LM, Zhu LF, Abliz B, Hu WJ, Zhong C, Bai ZG, Sajid H, Cao XC, Jin QY (2018) Hydrogen sulfide alleviates aluminum toxicity via decreasing apoplast sand symplast Al contents in rice. Front Plant Sci 9:294

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was partially supported by the University of Harran (Turkey).

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  1. Agriculture Faculty, Soil Science and Plant Nutrition Department, Harran University, Sanliurfa, Turkey

    Cengiz Kaya

  2. Pakistan Academy of Science, Islamabad, Pakistan

    Muhammad Ashraf

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  1. Cengiz Kaya
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  2. Muhammad Ashraf
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Correspondence to Cengiz Kaya.

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Kaya, C., Ashraf, M. The mechanism of hydrogen sulfide mitigation of iron deficiency-induced chlorosis in strawberry (Fragaria × ananassa) plants. Protoplasma 256, 371–382 (2019). https://doi.org/10.1007/s00709-018-1298-x

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  • DOI: https://doi.org/10.1007/s00709-018-1298-x

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