Skip to main content

Haem Oxygenase-1 is Involved in Hydrogen Sulfide-induced Cucumber Adventitious Root Formation

Abstract

Results from our previous study suggested that haem oxygenase-1/carbon monoxide (HO-1/CO) acts as a downstream signal system in the auxin-induced pathway leading to cucumber (Cucumis sativus) adventitious root formation. The objective of this study was to test whether HO-1 is also involved in hydrogen sulfide (H2S)-induced adventitious root formation. Cucumber explants were treated with HO-1 inducer haemin and H2S donor sodium hydrosulfide (NaHS) in combination with the specific inhibitor of HO-1 zinc protoporphyrin IX (ZnPPIX), and their effects on cucumber adventitious root development in IAA-depleted explants were compared. The results showed that similar to inducible responses of haemin, NaHS brought about the induction of cucumber HO-1 transcripts (CsHO-1) and its protein levels, and thereafter adventitious root formation. A further experiment verified that H2S or HS- rather than other sulfur-containing components derived from NaHS was ascribed to the stimulation response. The inducible effect is specific for CsHO-1 because ZnPPIX significantly suppressed the above responses, and the inhibitory effects were reversed partially when 30% CO-saturated aqueous solution was added. Molecular evidence further suggested that the NaHS-triggered upregulation of target genes responsible for HO-1/CO-induced adventitious root formation, including CsDNAJ-1 and CsCDPK1/5, was inhibited significantly by ZnPPIX. These decreases were reversed obviously by the addition of CO aqueous solution. However, hypotaurine (HT), the H2S scavenger, could not influence the haemin- and CO-induced adventitious rooting in IAA-depleted cucumber explants. Together, the above results suggested that HO-1 was involved in H2S-induced cucumber adventitious root formation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • Baraňano DE, Rao M, Ferris CD, Snyder SH (2002) Biliverdin reductase: a major physiologic cytoprotectant. Proc Natl Acad Sci USA 99:16093–16098

    Article  PubMed  Google Scholar 

  • Baskar R, Bian J (2011) Hydrogen sulfide gas has cell growth regulatory role. Eur J Pharmacol 656:5–9

    Article  PubMed  CAS  Google Scholar 

  • Cao ZY, Xuan W, Liu ZY, Li XN, Zhao N, Xu P, Wang Z, Guan RZ, Shen WB (2007) Carbon monoxide promotes lateral root formation in rapeseed. J Integr Plant Biol 49:1007–1016

    Article  Google Scholar 

  • Cao Z, Geng B, Xu S, Xuan W, Nie L, Shen W, Liang Y, Guan R (2011) BnHO1, a haem oxygenase-1 gene from Brassica napus, is required for salinity and osmotic stress-induced lateral root formation. J Exp Bot 62:4675–4689

    Article  PubMed  CAS  Google Scholar 

  • Davis SJ, Bhoo SH, Durski AM, Walker JM, Vierstra RD (2001) The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol 126:656–669

    Article  PubMed  CAS  Google Scholar 

  • de Montaigu A, Tóth R, Coupland G (2010) Plant development goes like clockwork. Trends Genet 26:296–306

    Article  PubMed  Google Scholar 

  • Dulak J, Józkowicz A (2003) Carbon monoxide—a “new” gaseous modulator of gene expression. Acta Biochim Pol 50:31–47

    PubMed  CAS  Google Scholar 

  • Frugis G, Mele G, Giannino D, Mariotti D (1999) MsJ1, an alfalfa DnaJ-like gene, is tissue-specific and transcriptionally regulated during cell cycle. Plant Mol Biol 40:397–408

    Article  PubMed  CAS  Google Scholar 

  • García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Han Y, Qin J, Chang XZ, Yang ZX, Du JB (2006) Hydrogen sulphide and carbon monoxide are in synergy with each other in the pathogenesis of recurrent febrile seizures. Cell Mol Neurobiol 26:101–107

    Article  PubMed  Google Scholar 

  • Kikuchi G, Yoshida T, Noguchi M (2005) Heme oxygenase and heme degradation. Biochem Biophys Res Commun 338:558–567

    Article  PubMed  CAS  Google Scholar 

  • Kumar KG, Ullanat R, Jayabaskaran C (2004) Molecular cloning, characterization, tissue-specific and phytohormone-induced expression of calcium-dependent protein kinase gene in cucumber (Cucumis sativus L.). J Plant Physiol 161:1061–1071

    Article  PubMed  CAS  Google Scholar 

  • Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Leffler CW, Parfenova H, Jaggar JH, Wang R (2006) Carbon monoxide and hydrogen sulfide: gaseous messengers in cerebrovasular circulation. J Appl Physiol 100:1065–1076

    Article  PubMed  CAS  Google Scholar 

  • Li L, Hsu A, Moore PK (2009a) Actions and interactions of nitric oxide, carbon monoxide and hydrogen sulphide in the cardiovascular system and in inflammation—a tale of three gases! Pharmacol Ther 123:386–400

    Article  PubMed  CAS  Google Scholar 

  • Li X, Bazer FW, Gao H, Jobqen W, Johnson GA, Li P, McKnight JR, Satterfield MC, Spencer TE, Wu G (2009b) Amino acids and gaseous signaling. Amino Acids 37:65–78

    Article  PubMed  Google Scholar 

  • Li MY, Cao ZY, Shen WB, Cui J (2011) Molecular cloning and expression of a cucumber (Cucumis sativus L.) heme oxygenase-1 gene, CsHO1, which is involved in adventitious root formation. Gene 486:47–55

    Article  PubMed  CAS  Google Scholar 

  • Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935

    Article  PubMed  CAS  Google Scholar 

  • Liu YH, Xu S, Ling TF, Xu LL, Shen WB (2010) Heme oxygenase/carbon monoxide system participates in regulating wheat seed germination under osmotic stress involving the nitric oxide pathway. J Plant Physiol 167:1371–1379

    Article  PubMed  CAS  Google Scholar 

  • Maines MD (1997) The heme oxygenase system: a regulator of second messenger genes. Annu Rev Pharmacol Toxicol 37:517–554

    Article  PubMed  CAS  Google Scholar 

  • Mancuso C, Navarra P, Preziosi P (2010) Roles of nitric oxide, carbon monoxide, and hydrogen sulfide in the regulation of the hypothalamic-pituitary-adrenal axis. J Neurochem 113:563–575

    Article  PubMed  CAS  Google Scholar 

  • Muramoto T, Kohchi T, Yokota A, Hwang I, Goodman HM (1999) The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11:335–348

    PubMed  CAS  Google Scholar 

  • Ortega JA, Ortega JM, Julian D (2008) Hypotaurine and sulfhydryl-containing antioxidants reduce H2S toxicity in erythrocytes from a marine invertebrate. J Exp Bot 211:3816–3825

    CAS  Google Scholar 

  • Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM (2000) Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6:422–428

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286

    Article  PubMed  CAS  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants—from the field to the test tube and back. Plant Biol 9:582–588

    Article  PubMed  CAS  Google Scholar 

  • Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583–650

    Article  PubMed  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  CAS  Google Scholar 

  • Shekhawat GS, Verma K (2010) Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. J Exp Bot 61:2255–2270

    Article  PubMed  CAS  Google Scholar 

  • Shekhawat GS, Dixit S, Verma K, Nasybullina EI, Kosmachevskaya OV, Topunov AF (2011) Heme oxygenase: enzyme with functional diversity. J Stress Physiol Biochem 7:88–94

    Google Scholar 

  • Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235:1043–1046

    Article  PubMed  CAS  Google Scholar 

  • Wang R (2003) The gasotransmitter role of hydrogen sulfide. Antioxid Redox Signal 5:493–501

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Wang YQ, Li L, Cui WT, Xu S, Shen WB, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119

    Article  CAS  Google Scholar 

  • Wu MZ, Huang JJ, Xu S, Ling TF, Xie YJ, Shen WB (2011) Haem oxygenase delays programmed cell death in wheat aleurone layers by modulation of hydrogen peroxide metabolism. J Exp Bot 62:235–248

    Article  PubMed  CAS  Google Scholar 

  • Xie YJ, Cui WT, Yuan XX, Shen WB, Yang Q (2011a) Heme oxygenase-1 is associated with wheat salinity acclimation by modulating reactive oxygen species homeostasis. J Integr Plant Biol 53:653–670

    Article  PubMed  CAS  Google Scholar 

  • Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011b) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role in RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Xuan W, Huang BK, Zhou YH, Ling TF, Xu S, Shen WB (2006) Carbon monoxide-induced adventitious rooting of hypocotyl cutting from mung bean seedling. Chin Sci Bull 51:668–674

    Article  CAS  Google Scholar 

  • Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Ye MB, Shen WB (2008) The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol 148:881–893

    Article  PubMed  CAS  Google Scholar 

  • Yannarelli GG, Noriega GO, Batlle A, Tomaro ML (2006) Heme oxygenase up-regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta 224:1154–1162

    Article  PubMed  CAS  Google Scholar 

  • Zhang QY, Du JB, Zhou WJ, Hui Y, Tang CS, Zhang CY (2004) Impact of hydrogen sulfide on carbon monoxide/heme oxygenase pathway in the pathogenesis of hypoxic pulmonary hypertension. Biochem Biophys Res Commun 317:30–37

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b) 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 H, Jiao H, Jiang CX, Wang SH, Wei ZJ, Luo JP, Jones RL (2010a) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 32:849–857

    Article  CAS  Google Scholar 

  • Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010b) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567

    Article  PubMed  CAS  Google Scholar 

  • Zhao W, Zhang J, Lu Y, Wang R (2001) The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO J 20:6008–6016

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Natural Science Foundation of Jiangsu Province of China (Grant No. BK2009309) and the Doctoral Fund of Ministry of Education of China (Grant No. 20100097110019).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wen-Biao Shen.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lin, YT., Li, MY., Cui, WT. et al. Haem Oxygenase-1 is Involved in Hydrogen Sulfide-induced Cucumber Adventitious Root Formation. J Plant Growth Regul 31, 519–528 (2012). https://doi.org/10.1007/s00344-012-9262-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-012-9262-z

Keywords

  • Adventitious rooting
  • Cucumber
  • Haem oxygenase-1
  • Hydrogen sulfide
  • Molecular mechanism