Skip to main content

Advertisement

SpringerLink
Log in

Hydrogen sulfide is a crucial element of the antioxidant defense system in Glycine max–Sinorhizobium fredii symbiotic root nodules

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aim

H2S is emerging as a signaling molecule involved in the regulation of many physiological processes in plants. Here, we investigated the potential antioxidant role of H2S in soybean (Glycine max)-rhizobia (Sinorhizobium fredii) symbiotic root nodules.

Method

An endogenous H2S production deficit rhizobia mutant ∆CSE was constructed to study the effect of decreased content of H2S in soybean nodules. Fluorescent probes and confocal microscope were used to observe the production and accumulation of H2S and reactive oxygen species. Transmission electronic microscopy was conducted to study the structural changes in ∆CSE soybean nodules. Finally, qRT-PCR, enzymatic activity, and oxidative damage parameters were measured.

Result

The results demonstrated that abundant H2S was generated in the nitrogen-fixing zone of soybean nodules. The deletion of the cystathionine γ-lyase (CSE) gene in S. fredii (∆CSE) caused a sharp decrease in H2S production in both free-living rhizobia and soybean nodules. We found that decrease in the H2S level in nodule cells inhibited nitrogenase activity. In addition, to elevated H2O2 and malondialdehyde accumulation, increased protein carbonyl content and decreased O2− scavenging ability was observed in ∆CSE root nodules. Transmission electron microscopy revealed that an H2S deficit caused the deformation of bacteroids and damage of peribacteroid membranes in nodule cells. Moreover, the expression of some rhizobial and soybean genes related to antioxidant defense was up-regulated in ∆CSE nodules.

Conclusion

H2S is crucial for the nitrogen-fixation ability of soybean nodules by acting as an antioxidant element that protects nodule cells and bacteroids from oxidative damage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Afendra AS, Drainas C (1987) Expression and stability of a recombinant plasmid in Zymomonas mobilis and Escherichia coli. J Gen Microbiol 133:127–134

    CAS  PubMed  Google Scholar 

  • Alesandrini F, Mathis R, Van de Sype G, Herouart D, Puppo A (2003) Possible roles for a cysteine protease and hydrogen peroxide in soybean nodule development and senescence. New Phytol 158:131–138

    CAS  Google Scholar 

  • Alvarez C, Calo L, Romero LC, García I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarez C, Garcia I, Moreno I, Esther Perez-Perez M, Crespo JL, Romero LC, Gotor C (2012) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aravind P, Prasad MNV (2005) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43:107–116

    CAS  PubMed  Google Scholar 

  • Aroca A, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol 168:334–342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aroca A, Benito JM, Gotor C, Romero LC, Kopriva S (2017a) Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis. J Exp Bot 68:4915–4927

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aroca A, Schneider M, Scheibe R, Gotor C, Romero LC (2017b) Hydrogen sulfide regulates the cytosolic/nuclear partitioning of Glyceraldehyde-3-phosphate dehydrogenase by enhancing its nuclear localization. Plant Cell Physiol 58:983–992

    CAS  PubMed  Google Scholar 

  • Aroca A, Gotor C, Romero LC (2018) Hydrogen sulfide signaling in plants: emerging roles of protein Persulfidation. Front Plant Sci 9:1621–1633

    Google Scholar 

  • Balestrasse KB, Gallego SM, Tomaro ML (2004) Cadmium-induced senescence in nodules of soybean ( Glycine max L.) plants. Plant Soil 262:373–381

    CAS  Google Scholar 

  • Becana M, Salin ML (1989) Superoxide dismutases in nodules of leguminous plants. Can J Bot 67:415–421

    CAS  Google Scholar 

  • Becana M, Dalton DA, Moran JF, Iturbe OI, Matamoros MA, Rubio MC (2001) Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381

    Google Scholar 

  • Becana M, Matamoros MA, Udvardi M, Dalton DA (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytol 188:960–976

    CAS  PubMed  Google Scholar 

  • Borsani O, Diaz P, Agius MF, Valpuesta V, Monza J (2001) Water stress generates an oxidative stress through the induction of a specific cu/Zn superoxide dismutase in Lotus corniculatus leaves. Plant Sci 161:757–763

    CAS  Google Scholar 

  • Cardenas L, Martinez A, Sanchez F, Quinto C (2008) Fast, transient and specific intracellular ROS changes in living root hair cells responding to nod factors (NFs). Plant J 56:802–813

    CAS  PubMed  Google Scholar 

  • Chen ZX, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic qcquired-resistance by slicylic-acid. Science 262:1883–1886

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Shang YT, Wang WH, Chen XY, He EM, Zheng HL, Shangguan ZP (2016) Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seedlings. Front Plant Sci 7:543–551

    Google Scholar 

  • Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng RY, Wang RR, Wang CY (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286

    CAS  PubMed  Google Scholar 

  • Chrysanthi K, Panagiotis K, Georgios K, Udvardi MK, Heinz R, Cornelia H, Emmanouil F (2015) Nitrogen-fixing nodules are an important source of reduced sulfur, which triggers global changes in sulfur metabolism in Lotus japonicus. Plant Cell 27:2384–2400

    Google Scholar 

  • Dalton DA (1995) Antioxidant defenses of plants and fungi. In: Ahmad S (ed) Oxidative stress and antioxidant defenses in biology. Springer, Boston, pp 298–355

    Google Scholar 

  • Dalton DA, Russell SA, Hanus F, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci U S A 83:3811–3815

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dalton DA, Langeberg L, Robbins M (1992) Purification and characterization of monodehydroascorbate reductase from soybean root nodules. Arch Biochem Biophys 292:281–286

    CAS  PubMed  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    CAS  Google Scholar 

  • Dickinson BC, Huynh C, Chang CJ (2010) A palette of fluorescent probes with varying emission colors for imaging hydrogen peroxide signaling in living cells. J Am Chem Soc 132:5906–5915

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dietz KJ (2010) Redox-dependent regulation, redox control and oxidative damage in plant cells subjected to abiotic stress. In: R Sunkar (ed) plant stress tolerance: methods and protocols. Humana press Totowa, pp 57-70

  • Evans PJ, Gallesi D, Mathieu C, Hernandez NJ, de Felipe N, Halliwell B, Puppo A (1999) Oxidative stress occurs during soybean nodule senescence. Planta 208:73–79

    CAS  Google Scholar 

  • Filipovic MR, Jovanovic VM (2017) More than just an intermediate: hydrogen sulfide signalling in plants. J Exp Bot 68:4733–4736

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    CAS  PubMed  Google Scholar 

  • Fishbeck K, Evans HJ, and Boersma LL (1973) Measurement of nitrogenase activity of intact legume symbionts in situ using the acetylene reduction assay. Agron J 65:429–433

  • Frendo P, Matamoros MA, Alloing G, Becana M (2013) Thiol-based redox signaling in the nitrogen-fixing symbiosis. Front Plant Sci 4:376–385

    PubMed  PubMed Central  Google Scholar 

  • Galatro A, González PM, Malanga G, Robello E, Piloni NE, Puntarulo S (2013) Nitric oxide and membrane lipid peroxidation in photosynthetic and non-photosynthetic organisms under several stress conditions. Front Physiol 4:276–278

    PubMed  PubMed Central  Google Scholar 

  • Galton MM, Hess ME (1946) Hydrogen Sulfide Formation by Shigella alkalescens. J Bacteriol 52:143–147

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gombos Z, Wada H, Murata N (1994) The recovery of photosynthesis from low-reperature photoinhibition is accelerated by the unsaturation of membrane-lipid-a mechanism fo chilling tollerance. Proc Natl Acad Sci U S A 91:8787–8791

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grosshennig S, Ischebeck T, Gibhardt J, Busse J, Feussner I, Stulke J (2016) Hydrogen sulfide is a novel potential virulence factor of Mycoplasma pneumoniae: characterization of the unusual cysteine desulfurase/desulfhydrase HapE. Mol Microbiol 100:42–54

    CAS  PubMed  Google Scholar 

  • Groten K, Dutilleul C, Heerden PDR, Vanacker H, Bernard S, Finkemeier I, Dietz K-J, Foyer CH (2006) Redox regulation of peroxiredoxin and proteinases by ascorbate and thiols during pea root nodule senescence. FEBS Lett 580:1269–1276

    CAS  PubMed  Google Scholar 

  • Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580

    CAS  PubMed  Google Scholar 

  • Hanyu M, Fujimoto H, Tejima K, Saeki K (2009) Functional differences of two distinct catalases in Mesorhizobium loti MAFF303099 under free-living and symbiotic conditions. J Bacteriol 191:1463–1471

    CAS  PubMed  Google Scholar 

  • Harrison A, Bakaletz LO, Jr MR (2012) Haemophilus influenzae and oxidative stress. Front Cell Infect Microbiol 2:40–50

    PubMed  PubMed Central  Google Scholar 

  • Herbette S, Lenne C, Leblanc N, Julien JL, Drevet JR, Roeckel-Drevet P (2002) Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. EJBio 269:2414–2420

    CAS  Google Scholar 

  • Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Biol 44:483–511

    CAS  Google Scholar 

  • Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Ii RMR, Peterson KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175–176

    CAS  PubMed  Google Scholar 

  • Laureano-Marín AM, Moreno I, Romero LC, Gotor C (2016) Negative regulation of autophagy by sulfide in Arabidopsis thaliana is independent of reactive oxygen species. Plant Physiol 171:1378–1391

    PubMed  PubMed Central  Google Scholar 

  • Lee MY, Shin KH, Kim YK, Suh JY, Gu YY, Kim MR, Hur YS, Son O, Kim JS, Song E, Lee MS, Nam KH, Sung MK, Kim HJ, Chun JY, Park M, Ahn TI, Hong CB, Lee SH, Park HJ, Park JS, Verma DPS, Cheon CI (2005) Induction of thioredoxin is required for nodule development to reduce reactive oxygen species levels in soybean roots. Plant Physiol 139:1881–1889

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li YX, Zhou L, Li YG, Chen DS, Tan XJ, Lei L, Zhou JC (2008) A nodule-specific plant cysteine proteinase, AsNODF32, is involved in nodule senescence and nitrogen fixation activity of the green manure legume Astragalus sinicus. New Phytol 180:185–192

    CAS  PubMed  Google Scholar 

  • Li L, Wang YQ, Shen WB (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. BioMetals 25:617–631

    CAS  PubMed  Google Scholar 

  • Lin VS, Lippert AR, Chang CJ (2013) Cell-trappable fluorescent probes for endogenous hydrogen sulfide signaling and imaging H2O2-dependent H2S production. Proc Natl Acad Sci U S A 110:7131–7135

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36:1607–1616

    CAS  PubMed  Google Scholar 

  • Liu HT, Naismith JH (2008) An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol 8:91–107

    PubMed  PubMed Central  Google Scholar 

  • Matamoros MA, Baird LM, Escuredo PR, Dalton DA, Minchin FR, Iturbe-Ormaetxe I, Rubio MC, Moran JF, Gordon AJ, Becana M (1999) Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol 121:97–112

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumura H, Miyachi S (1980) Cycling assay for nicotinamide adenine dinucleotides. Methods Enzymol 69:465–470

    CAS  Google Scholar 

  • Mironov A, Seregina T, Nagornykh M, Luhachack LG, Korolkova N, Lopes LE, Kotova V, Zavilgelsky G, Shakulov R, Shatalin K (2017) Mechanism of H2S-mediated protection against oxidative stress in Escherichia coli. Proc Natl Acad Sci U S A 114:6022

    CAS  PubMed  PubMed Central  Google Scholar 

  • Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    PubMed  Google Scholar 

  • Mouradi M, Farissi M, Bouizgaren A, Qaddoury A, Ghoulam C (2018) Medicago sativa-rhizobia symbiosis under water deficit: physiological, antioxidant and nutritional responses in nodules and leaves. J Plant Nutr 41:384–395

    CAS  Google Scholar 

  • Naya L, Ladrera R, Ramos J, Gonzalez EM, Arrese-Igor C, Minchin FR, Becana M (2007) The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiol 144:1104–1114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Panek HR, O'Brian MR (2004) KatG is the primary detoxifier of hydrogen peroxide produced by aerobic metabolism in Bradyrhizobium japonicum. J Bacteriol 186:7874–7880

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pekker I, Tel-Or E, Mittler R (2002) Reactive oxygen intermediates and glutathione regulate the expression of cytosolic ascorbate peroxidase during iron-mediated oxidative stress in bean. Plant Mol Biol 49:429–438

    CAS  PubMed  Google Scholar 

  • Peng H, Zhang Y, Palmer LD, Kehl-Fie TE, Skaar EP, Trinidad JC, Giedroc DP (2017) Hydrogen sulfide and reactive sulfur species impact proteome S-sulfhydration and global virulence regulation in Staphylococcus aureus. ACS Infect Dis 3:744–755

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qu K, Lee SW, Bian JS, Low CM, Wong PT (2008) Hydrogen sulfide: neurochemistry and neurobiology. Neurochem Int 52:155–165

    CAS  PubMed  Google Scholar 

  • Ramirez M, Iniguez LP, Guerrero G, Sparvoli F, Hernandez G (2016) Rhizobium etli bacteroids engineered for Vitreoscilla hemoglobin expression alleviate oxidative stress in common bean nodules that reprogramme global gene expression. Plant Biotechnol Rep 10:463–474

    Google Scholar 

  • Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509

    CAS  PubMed  Google Scholar 

  • Reibach PH, Mask PL, Streeter JG, (1981) A rapid one-step method for the isolation of bacteroids from root nodules of soybean plants, utilizing self-generating Percoll gradients. Can J Microbiol 27(5):491–495

  • Redondo FJ, de la Pena TC, Morcillo CN, Lucas MM, Pueyo JJ (2009) Overexpression of flavodoxin in bacteroids induces changes in antioxidant metabolism leading to delayed senescence and starch accumulation in alfalfa root nodules. Plant Physiol 149:1166–1179

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ribera-Fonseca A, Inostroza-Blancheteau C, Cartes P, Rengel Z, Mora ML (2013) Early induction of Fe-SOD gene expression is involved in tolerance to Mn toxicity in perennial ryegrass. Plant Physiol Biochem 73:77–82

    CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, Palma JM, Gomez M, Del Rio LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686

    CAS  Google Scholar 

  • Rubio MC, James EK, Clemente MR, Bucciarelli B, Fedorova M, Vance CP, Becana M (2004) Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Mol Plant-Microbe Interact 17:1294–1305

    CAS  PubMed  Google Scholar 

  • Saegesser R, Ghosh R, Bachofen R (1992) Stability of broad host range cloning vectors in the photorophic bacterium Phodospirillum rubrum. FEMS Microbiol Lett 95:7–12

    CAS  Google Scholar 

  • Sandalio LM, Rodriguez-Serrano M, del Rio LA, Romero-Puertas MC (2009) Reactive oxygen species and signaling in cadmium toxicity. In: DelRio LA, Puppo A (eds) Reactive oxygen species in plant signaling. Springer, Berlin, pp 175–189

    Google Scholar 

  • Santos R, Hérouart D, Puppo A, Touati D (2000) Critical protective role of bacterial superoxide dismutase in rhizobium-legume symbiosis. Mol Microbiol 38:750–759

    CAS  PubMed  Google Scholar 

  • Santos R, Herouart D, Sigaud S, Touati D, Puppo A (2001) Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol Plant-Microbe Interact 14:86–89

    CAS  PubMed  Google Scholar 

  • Shatalin K, Shatalina E, Mironov A, Nudler E (2011) H2S: a universal defense against antibiotics in bacteria. Science 334:986–990

    CAS  PubMed  Google Scholar 

  • Shi HT, Ye TT, Chan ZL (2013) Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 71:226–234

    CAS  PubMed  Google Scholar 

  • Shulaev V, Oliver DJ (2006) Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol 141:367–372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soutourina O, Dubrac S, Poupel O, Msadek T, Martin Verstraete I (2010) The pleiotropic CymR regulator of Staphylococcus aureus plays an important role in virulence and stress response. PLoS Pathog 6:e1000894

    PubMed  PubMed Central  Google Scholar 

  • Szabó (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6:917–935

    PubMed  Google Scholar 

  • Vargas MC, Encarnación S, Dávalos A, Reyes-Pérez A, Mora Y, García-De LSA, Brom S, Mora J (2003) Only one catalase, katG, is detectable in Rhizobium etli, and is encoded along with the regulator OxyR on a plasmid replicon. Microbiology 149:1165

    CAS  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

    CAS  PubMed  Google Scholar 

  • Wang BL, Shi L, Li YX, ZHang WH (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber ( Cucumis sativus L.) seedlings. Planta 231:1301–1309

    CAS  PubMed  Google Scholar 

  • Wu GF, Li N, Mao YT, Zhou GQ, Gao HC (2015) Endogenous generation of hydrogen sulfide and its regulation in Shewanella oneidensis. Front Microbiol 6:169–188

    Google Scholar 

  • Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang GD, Wu LY, Jiang B, Yang W, Qi JS, Cao K, Meng QH, Mustafa AK, Mu WT, Zhang SM, Snyder SH, Wang R (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase. Science 322:587–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, Z, Zhang Z, Wang X, Li L, Cai K, Han H (2017) Novel impacts of functionalized multi-walled carbon nanotubes in plants: promotion of nodulation and nitrogenase activity in the rhizobium-legume system. Nanoscale 9 (28):9921–9937

  • Špirić Z, Stafilov T, Vučković I, Glad M (2014) Study of nitrogen pollution in Croatia by moss biomonitoring and Kjeldahl method. J Environ Sci Health A 49 (12):1402–1408

  • Zhang H, Tang J, Liu XP, Wang Y, Yu W (2008) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094

  • Zhang H, Tang J, Liu XP, Wang Y, Yu W (2009) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094

  • Zou H, Zhang N-N, Pan Q, Zhang J-H, Chen J, Wei G-H (2019) Hydrogen sulfide promotes nodulation and nitrogen fixation in soybean–rhizobia symbiotic system.Mol Plant-Microbe Interact 32:972–985

Download references

Acknowledgments

We are grateful for the kind help provided by Yan-Qing Wang and Ke-Rang Huang for microscopy analysis. This work was supported by the Natural Science Foundationof China (31501822 and 41830755) and the Postdoctoral Science Foundation of China (2015 M580876 and 2016 T90948).

Author information

Author notes

  1. Hang Zou and Ni-Na Zhang contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology in Arid Areas, College of life sciences, Northwest A&F University, 3 Taicheng Road, Yangling, Shaanxi, 712100, People’s Republic of China

    Hang Zou, Juan Chen & Ge-Hong Wei

  2. Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, Yangling, Shaanxi, 712100, People’s Republic of China

    Hang Zou & Ge-Hong Wei

  3. State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, Shaanxi, 712100, People’s Republic of China

    Ni-Na Zhang, Xue-Yuan Lin, Wei-Qin Zhang & Juan Chen

  4. School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong, People’s Republic of China

    Jian-Hua Zhang

  5. Department of Biology, Hong Kong Baptist University, Hong Kong, People’s Republic of China

    Jian-Hua Zhang

Authors
  1. Hang Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ni-Na Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xue-Yuan Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wei-Qin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian-Hua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Juan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ge-Hong Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Juan Chen or Ge-Hong Wei.

Additional information

Responsible Editor: Ulrike Mathesius.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 321 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zou, H., Zhang, NN., Lin, XY. et al. Hydrogen sulfide is a crucial element of the antioxidant defense system in Glycine max–Sinorhizobium fredii symbiotic root nodules. Plant Soil 449, 209–231 (2020). https://doi.org/10.1007/s11104-020-04465-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-020-04465-9

Keywords

Search

Navigation