Abstract
Our previous results showed that β-cyclodextrin–hemin complex (CDH) exhibited a vital protective role against cadmium-induced oxidative damage and toxicity in alfalfa seedling roots by the regulation of heme oxygenase-1 (HO-1) gene expression. In this report, we further test whether CDH exhibited the hormonal-like response. The application of CDH and an inducer of HO-1, hemin, were able to induce the up-regulation of cucumber HO-1 gene (CsHO1) expression and thereafter the promotion of adventitious rooting in cucumber explants. The effect is specific for HO-1 since the potent HO-1 inhibitor zinc protoporphyrin IX (ZnPP) blocked the above responses triggered by CDH, and the inhibitory effects were reversed further when 30 % saturation of CO aqueous solution was added together. Further, molecular evidence showed that CDH triggered the increases of the HO-1-mediated target genes responsible for adventitious rooting, including one DnaJ-like gene (CsDNAJ-1) and two calcium-dependent protein kinase (CDPK) genes (CsCDPK1 and CsCDPK5), and were inhibited by ZnPP and reversed by CO. The calcium (Ca2+) chelator ethylene glycol-bis (2-aminoethylether)-N,N,N′,N′-tetraacetic acid (EGTA) and the Ca2+ channel blocker lanthanum chloride (LaCl3) not only compromised the induction of adventitious rooting induced by CDH but also decreased the transcripts of above three target genes. However, the application of ascorbic acid (AsA), a well-known antioxidant in plants, failed to exhibit similar inducible effect on adventitious root formation. In short, above results illustrated that the response of CDH in the induction of cucumber adventitious rooting might be through HO-1-dependent mechanism and calcium signaling.
Key message Physiological, pharmacological and molecular evidence showed that β-cyclodextrin–hemin complex (CDH) was able to induce cucumber adventitious rooting through heme oxygenase-1 (HO-1)-dependent mechanism and calcium signaling.
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References
Bai X, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-oxo-decanoyl-l-homoserine-lactone activates auxin-induced adventitious root formation via H2O2- and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiol 158:725–736
Bauer M, Huse K, Settmacher U, Claus RA (2008) The heme oxygenase–carbon monoxide system: regulation and role in stress response and organ failure. Intensive Care Med 34:640–648
Bellamine J, Penel C, Greppin H, Gaspar T (1998) Confirmation of the role of auxin and calcium in the late phases of adventitious root formation. Plant Growth Regul 26:191–194
Cao ZY, Huang BK, Wang QY, Xuan W, Ling TF, Zhang B, Chen X, Nie L, Shen W (2007a) Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway. Chinese Sci Bull 52:2365–2373
Cao ZY, Xuan W, Liu ZY, Li XN, Zhao N, Xu P, Wang Z, Guan RZ, Shen WB (2007b) Carbon monoxide promotes lateral root formation in rapeseed. J Integr Plant Biol 49:1070–1079
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
Chen YH, Kao CH (2012) Calcium is involved in nitric oxide- and auxin-induced lateral root formation in rice. Protoplasma 249:187–195
Chen YH, Chao YY, Hsu YY, Hong CY, Kao CH (2012) Heme oxygenase is involved in nitric oxide- and auxin-induced lateral root formation in rice. Plant Cell Rep. doi:10.1007/s00299-012-1228-x
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
Dellon ES, Szczepiorkowski ZM, Dzik WH, Grame-Cook F, Ades A, Bloomer JR, Cosimi AB, Chung RT (2002) Treatment of recurrent allograft dysfunction with intravenous haematin after liver transplantation for erythropoietic protoporphyria. Transplantation 73:911–915
Den Herder G, Van Isterdael G, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends Plant Sci 15:600–607
Devadas K, Dhawan S (2006) Hemin activation ameliorates HIV-1 infection via heme oxygenase-1 induction. J Immunol 176:4252–4257
Dulak J, Józkowicz A (2003) Carbon monoxide–a “new” gaseous modulator of gene expression. Acta Biochim Pol 50:31–47
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
Fu GQ, Zhang LF, Cui WT, Wang YQ, Shen WB, Ren Y, Zheng TQ (2011) Induction of heme oxygenase-1 with β-CD-hemin complex mitigates cadmium-induced oxidative damage in the roots of Medicago sativa. Plant Soil 345:271–285
Han Y, Zhang J, Chen X, Gao Z, Xuan W, Xu S, Ding X, Shen W (2008) Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. New Phytol 177:155–166
Han B, Xu S, Xie YJ, Huang JJ, Wang LJ, Yang Z, Zhang CH, Sun Y, Shen WB, Xie GS (2012) ZmHO-1, a maize haem oxygenase-1 gene, plays a role in determining lateral root development. Plant Sci 184:63–74
Huang YP, Cai RX, Mao LY, Liu ZH, Huang HP (1999) Spectrophotometric determination of hydrogen peroxide using β-CD-Hemin as a mimetic enzyme of peroxidase. Anal Sci 15:889–894
Huang J, Han B, Xu S, Zhou M, Shen W (2011) Heme oxygenase-1 is involved in the cytokinin-induced alleviation of senescence in detached wheat leaves during dark incubation. J Plant Physiol 168:768–775
Jung YD, Chay KO, Song DU, Moon JS, Yang SY, Lee MW, Ahn BW (1997) Hemin inhibits lipid peroxidation induced by ascorbate/FeSO4 and 2,2′-azobis-2-amidino-propane hydrochloride (ABAP). Exp Mol Med 29:171–175
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
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
Lanteri ML, Laxalt AM, Lamattina L (2008) Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol 147:188–198
Li SW, Xue L, Xu S, Feng H, An L (2009) Hydrogen peroxide acts as a signal molecule in the adventitious root formation of mung bean seedlings. Environ Exp Bot 65:63–71
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
Lin YT, Li MY, Cui WT, Lu W, Shen WB (2012) Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation. J Plant Growth Regul. doi:10.1007/s00344-012-9262-z
Liu ZH, Cai RX, Mao LY, Huang HP, Ma WH (1999) Highly sensitive spectrofluorimetric determination of hydrogen peroxide with β-cyclodextrin–hemin as catalyst. Analyst 124:173–176
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
Noriega GO, Balestrasse KB, Batlle A, Tomaro ML (2004) Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochem Biophys Res Commun 323:1003–1008
Otterbein LE, Soares MP, Yamashita K, Bach FH (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449–455
Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956
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
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
Ryter SW, Otterbein LE, Morse D, Choi AMK (2002) Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem 234\235(1–2):249–263
Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583–650
Shekhawat GS, Verma K (2010) Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. J Exp Bot 61:2255–2270
Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, Geiss G, McKhann H, Garcion C, Vaucheret H, Sandberg G, Bellini C (2005) Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17:1343–1359
Ullanat R, Jayabaskaran C (2002) Distinct light-, cytokinin-, and tissue-specific regulation of calcium-dependent protein kinase gene expression in cucumber (Cucumis sativus). Plant Sci 162:153–163
Wen T, Wu ZM, Liu Y, Tan YF, Ren F, Wu H (2007) Upregulation of heme oxygenase-1 with hemin prevents d-galactosamine and lipopolysaccharide-induced acute hepatic injury in rats. Toxicology 237:184–193
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
Xie YJ, Ling TF, Han Y, Liu KL, Zheng QS, Huang LQ, Yuan XX, He ZY, Hu B, Fang L, Shen ZG, Yang Q, Shen WB (2008) Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots. Plant, Cell Environ 31:1864–1881
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
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
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. Chinese Sci Bull 51:668–674
Xu DK, Jin QJ, Xie YJ, Liu YH, Lin YT, Shen WB, Zhou YJ (2011a) Characterization of a wheat heme oxygenase-1 gene and its response to different abiotic stresses. Int J Mol Sci 12:7692–7707
Xu S, Lou TL, Zhao N, Gao Y, Dong LH, Jiang DJ, Shen WB, Huang LQ, Wang R (2011b) Presoaking with hemin improves salinity tolerance during wheat seed germination. Acta Physiol Plant 33:1173–1183
Xuan W, Huang LQ, Li M, Huang BK, Xu S, Liu H, Gao Y, Shen WB (2007) Induction of growth elongation in wheat root segments by heme molecules: a regulatory role of carbon monoxide in plants? Plant Growth Regul 52:41–51
Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY, 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
Zilli CG, Santa-Cruz DM, Yannarelli GG, Noriega GO, Tomaro ML, Balestrasse KB (2009) Heme oxygenase contributes to alleviate salinity damage in Glycine max L. leaves. Int J Cell Biol 2009:848516
Acknowledgments
This work was supported by the Doctoral Fund of Ministry of Education of China (grant no. 20100097110019), the Natural Science Foundation of Jiangsu Province of China (grant no. BK2009309), and the Technology Support Program in Jiangsu Province, China (grant no. BE2010382).
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Communicated by P. Kumar.
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Lin, Y., Li, M., Huang, L. et al. Involvement of heme oxygenase-1 in β-cyclodextrin–hemin complex-induced cucumber adventitious rooting process. Plant Cell Rep 31, 1563–1572 (2012). https://doi.org/10.1007/s00299-012-1270-8
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DOI: https://doi.org/10.1007/s00299-012-1270-8