| Peer-Reviewed

Hydrogen Sulphide Improves Iron Homeostasis in Wheat Under Iron-Deficiency

Received: 9 October 2017    Accepted: 20 October 2017    Published: 24 November 2017
Views:       Downloads:
Abstract

Hydrogen sulphide (H2S) is emerging as an important gaseous molecule involved in various plant developmental processes and plant stress responses. In this study, exogenous H2S donor (sodium hydrosulfide, NaHS) treated wheat plants were used to investigate the role of H2S in response to iron-deficiency. The results showed that H2S significantly alleviated leaf chlorosis under iron-deficient conditions, and thus improved photosynthesis. Moreover, H2S increased the lateral root (LR) number, density and length of wheat seedlings grown in iron-sufficient and deficient culture solution, and promoted phytosiderophores (PSs) secretion from roots simultaneously, which eventually led to an increase in iron uptake. Taken together, these results indicate that H2S improved iron uptake by regulating root development and PSs secretion, and consequently increased chlorophyll biosynthesis and photosynthesis in plants under iron-deficiency.

Published in Journal of Plant Sciences (Volume 5, Issue 6)
DOI 10.11648/j.jps.20170506.11
Page(s) 170-176
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Hydrogen Sulfide, Iron-Deficiency, Phytosiderophores, Lateral Root, Wheat

References
[1] Vose PB (1982) Iron nutrition in plants: a world overview. J Plant Nutr 5:233-249.
[2] Schmidt (2003) Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci 8:188-193.
[3] Jin CW, Du ST, Chen WW, Li GX, Zhang YS, Zheng S J (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.
[4] Jin CW, Liu Y, Mao QQ, Wang Q, Du S T (2013a). Mild Fe-deficiency improves biomass production and quality of hydroponic-cultivated spinach plants (Spinacia oleracea L.). Food chem 138:2188-2194.
[5] Takahashi M, Nakanishi H, Kawasaki S, 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.
[6] Walker EL and Connolly EL (2008) Time to pump iron: iron-deficiency-signaling mechanisms of higher plants. Curr Opin Plant Biol 11:530-535.
[7] Graziano M, Beligni M V, Lamattina L. Nitric oxide improves internal iron availability in plants. Plant Physiol. 2002, 130: 1852-1859.
[8] Kong WW, Zhang LP. Guo K, Liu ZP, Yang ZM (2010) Carbon monoxide improves adaptation of Arabidopsis to iron deficiency. Plant Biotechnol J 8:88-99.
[9] Li C, Zhu X, Zhang F (2000) Role of shoot in regulation of iron deficiency responses in cucumber and bean plants. J Plant Nutr 23:1809-1818.
[10] Li X, Li C (2004) Is ethylene involved in regulation of root ferric reductase activity of dicotyledonous species under iron deficiency. Plant Soil 261:147-153.
[11] Zheng SJ, Tang CX, Arakama Y, Masaoka Y (2003) The responses of red clover (Trifolium pratense L.) to iron deficiency: a root Fe (III) chelate reductase. Plant Sci 164:679-687.
[12] Lingam S, Mohrbacher J, Brumbarova T, Potuschak T, Fink-Straube C, Blondet E, Genschik P, Bauer P (2011) Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23: 1815-1829.
[13] Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792-1798.
[14] Olson KR (2009) Is hydrogen sulfide a circulating “gasotransmitter” in vertebrate blood? BBA-Bioenergetics 1787:856-863.
[15] Tan BH, Wong PTH, Bian JS (2010) Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56:3-10.
[16] Lisjak M, Teklić T, Wilson ID, Wood M, Whiteman M, Hancock JT (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signal Behav 6:1444-1446.
[17] Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013b) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Bioch 62:41-46
[18] Dooley FD, Nair SP, Ward PD (2013) Increased growth and germination success in plants following hydrogen sulfide administration. Plos one 8:e62048
[19] Xie Y, Zhang C, Lai D, Sun Y, Samma MK, Zhang J, Shen W (2014) Hydrogen sulfide delays GA-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression. J Plant Physiol 171:53-62.
[20] Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518-1529.
[21] Zhang H, Hu LY, Li P, Hu KD, Jiang CX, Luo JP (2010a) Hydrogen sulfide alleviated chromium toxicity in wheat. Biol Plantarum 54:743-747.
[22] Zhang H, Jiao H, Jiang CX, Wang SH, Wei ZJ, Luo JP, Jones RL (2010b) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 32:849-857.
[23] Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564-1572.
[24] Li H, Gao MQ, Xue RL, Wang D, Zhao HJ (2015) Effect of hydrogen sulfide on D1 protein in wheat under drought stress. Acta Physiol Plant 37:225.
[25] Shi H, Ye T, Chan Z (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74: 99-107.
[26] Fang T, Cao Z, Li J, Shen W, Huang L (2014) Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol Bioch 76:44-51.
[27] Jia H, Hu Y, Fan T, Li J (2015) Hydrogen sulfide modulates actin-dependent auxin transport via regulating ABPs results in changing of root development in Arabidopsis. Sci Rep-UK 5: srep08251.
[28] Hou ZH, Wang LX, Liu J, Hou LX, Liu X (2013) Hydrogen Sulfide Regulates Ethylene-induced Stomatal Closure in Arabidopsis thaliana. J Integr Plant Biol 55:277-289.
[29] Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng 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.
[30] Duan B, Ma Y, Jiang M, Yang F, Ni L, Lu W (2015) Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment. Plant Growth Regul 75:33-44.
[31] 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 defence pathways. J Exp Bot 64:1953-1966.
[32] Mostofa MG, Rahman A, Ansary MMU, Watanabe A, Fujita M, Tran LSP (2015) Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep 5:14078.
[33] Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350-382.
[34] Reichman SM, Parker DR (2007) Critical evaluation of three indirect assays for quantifying phytosiderophores released by the roots of Poaceae. Eur J Soil Sci 58:844-853.
[35] Ali S, Farooq MA, Hussain S, Yasmeen T, Abbasi GH, Zhang G (2013) Alleviation of chromium toxicity by hydrogen sulfide in barley. Environ Toxicol Chem 32:2234-2239.
[36] Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, Ahmad MSA (2014) Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut R 21:717-731.
[37] Marschner H, Römheld V, Kissel M (1986) Different strategies in higher plants in mobilization and uptake of iron. J Plant Nutr 9:695-713.
[38] Moog PR, Kooij TA, Brüggemann W, Schiefelbein JW, Kuiper PJ (1995) Responses to iron deficiency in Arabidopsis thaliana: the turbo iron reductase does not depend on the formation of root hairs and transfer cells. Planta 195:505-513.
[39] Dasgan HY, Römheld V, Cakmak I, Abak K (2002) Physiological root responses of iron deficiency susceptible and tolerant tomato genotypes and their reciprocal F1 hybrids. Plant Soil 241:97-104.
[40] Jin CW, Chen WW, Meng ZB, Zheng SJ (2008) Iron Deficiency-induced increase of root branching contributes to the enhanced root ferric chelate reductase activity. J Integr Plant Biol 50:1557-1562.
[41] Jin CW, Du ST, Shamsi IH, Luo BF, Lin X Y (2011) NO synthase-generated NO acts downstream of auxin in regulating Fe-deficiency-induced root branching that enhances Fe-deficiency tolerance in tomato plants. J Exp Bot 62:3875-3884.
[42] Xue YF, Zhang M, Qi ZQ, Li YQ, Shi, Chen J (2016) Cinnamaldehyde promotes root branching by regulating endogenous hydrogen sulfide. J Sci Food Agr 96:909-914.
[43] Gries D, Brunn S, Crowley DE, Parker DR (1995) Phytosiderophore release in relation to micronutrient metal deficiencies in barley. Plant Soil 172:299-308.
[44] Chaignon V, Di Malta D, Hinsinger P (2002) Fe-deficiency increases Cu acquisition by wheat cropped in a Cu-contaminated vineyard soil. New Phytol 154:121-130.
[45] Meda AR, Scheuermann EB, Prechsl UE, Erenoglu B, Schaaf G, Hayen H, Weber G, von Wirén N (2007) Iron acquisition by phytosiderophores contributes to cadmium tolerance. Plant Physiol 143:1761-1773.
[46] Neelam K, Tiwari VK, Rawat N, Tripathi SK, Randhawa GS, Dhaliwal HS (2010) Identification of Aegilops species with higher production of phytosiderophore and iron and zinc uptake under micronutrient-sufficient and-deficient conditions. Plant Genet Resour-C 8: 132-141.
[47] Bocchini M, Bartucca ML, Ciancaleoni S, Mimmo T, Cesco S, Pii Y, Albertini E, Del Buono D (2015) Iron deficiency in barley plants: phytosiderophore release, iron translocation, and DNA methylation. Front Plant Sci 6.
Cite This Article
  • APA Style

    Xia Zhang, Yang Zhang, Lu Zhang, Huijie Zhao, Hua Li. (2017). Hydrogen Sulphide Improves Iron Homeostasis in Wheat Under Iron-Deficiency. Journal of Plant Sciences, 5(6), 170-176. https://doi.org/10.11648/j.jps.20170506.11

    Copy | Download

    ACS Style

    Xia Zhang; Yang Zhang; Lu Zhang; Huijie Zhao; Hua Li. Hydrogen Sulphide Improves Iron Homeostasis in Wheat Under Iron-Deficiency. J. Plant Sci. 2017, 5(6), 170-176. doi: 10.11648/j.jps.20170506.11

    Copy | Download

    AMA Style

    Xia Zhang, Yang Zhang, Lu Zhang, Huijie Zhao, Hua Li. Hydrogen Sulphide Improves Iron Homeostasis in Wheat Under Iron-Deficiency. J Plant Sci. 2017;5(6):170-176. doi: 10.11648/j.jps.20170506.11

    Copy | Download

  • @article{10.11648/j.jps.20170506.11,
      author = {Xia Zhang and Yang Zhang and Lu Zhang and Huijie Zhao and Hua Li},
      title = {Hydrogen Sulphide Improves Iron Homeostasis in Wheat Under Iron-Deficiency},
      journal = {Journal of Plant Sciences},
      volume = {5},
      number = {6},
      pages = {170-176},
      doi = {10.11648/j.jps.20170506.11},
      url = {https://doi.org/10.11648/j.jps.20170506.11},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.jps.20170506.11},
      abstract = {Hydrogen sulphide (H2S) is emerging as an important gaseous molecule involved in various plant developmental processes and plant stress responses. In this study, exogenous H2S donor (sodium hydrosulfide, NaHS) treated wheat plants were used to investigate the role of H2S in response to iron-deficiency. The results showed that H2S significantly alleviated leaf chlorosis under iron-deficient conditions, and thus improved photosynthesis. Moreover, H2S increased the lateral root (LR) number, density and length of wheat seedlings grown in iron-sufficient and deficient culture solution, and promoted phytosiderophores (PSs) secretion from roots simultaneously, which eventually led to an increase in iron uptake. Taken together, these results indicate that H2S improved iron uptake by regulating root development and PSs secretion, and consequently increased chlorophyll biosynthesis and photosynthesis in plants under iron-deficiency.},
     year = {2017}
    }
    

    Copy | Download

  • TY  - JOUR
    T1  - Hydrogen Sulphide Improves Iron Homeostasis in Wheat Under Iron-Deficiency
    AU  - Xia Zhang
    AU  - Yang Zhang
    AU  - Lu Zhang
    AU  - Huijie Zhao
    AU  - Hua Li
    Y1  - 2017/11/24
    PY  - 2017
    N1  - https://doi.org/10.11648/j.jps.20170506.11
    DO  - 10.11648/j.jps.20170506.11
    T2  - Journal of Plant Sciences
    JF  - Journal of Plant Sciences
    JO  - Journal of Plant Sciences
    SP  - 170
    EP  - 176
    PB  - Science Publishing Group
    SN  - 2331-0731
    UR  - https://doi.org/10.11648/j.jps.20170506.11
    AB  - Hydrogen sulphide (H2S) is emerging as an important gaseous molecule involved in various plant developmental processes and plant stress responses. In this study, exogenous H2S donor (sodium hydrosulfide, NaHS) treated wheat plants were used to investigate the role of H2S in response to iron-deficiency. The results showed that H2S significantly alleviated leaf chlorosis under iron-deficient conditions, and thus improved photosynthesis. Moreover, H2S increased the lateral root (LR) number, density and length of wheat seedlings grown in iron-sufficient and deficient culture solution, and promoted phytosiderophores (PSs) secretion from roots simultaneously, which eventually led to an increase in iron uptake. Taken together, these results indicate that H2S improved iron uptake by regulating root development and PSs secretion, and consequently increased chlorophyll biosynthesis and photosynthesis in plants under iron-deficiency.
    VL  - 5
    IS  - 6
    ER  - 

    Copy | Download

Author Information
  • College of Life Science, Henan Agricultural University, Zhengzhou, China

  • College of Life Science, Henan Agricultural University, Zhengzhou, China

  • College of Life Science, Henan Agricultural University, Zhengzhou, China

  • College of Life Science, Henan Agricultural University, Zhengzhou, China

  • College of Life Science, Henan Agricultural University, Zhengzhou, China

  • Sections