Heme oxygenase 1 and abiotic stresses in plants

• Autorzy: He H. , He H.
• Języki publikacji: EN

Abstrakty

EN

As a key enzyme of heme degradation, heme oxygenase (HO) is essential in phytochrome chromophore synthesis, cell protection and stomatal regulation in higher plants. The activity or transcript of HO has been detected in many plant species. Arabidopsis HO1 (HY1), the first map-based cloning gene, could catalyze the transition of heme to carbon monoxide (CO) in vivo. In this review, we first describe HO1 is evolutionarily conserved through comparative analysis of different plants HO1 proteins. Then, we highlight the role of HO1 involved in plants responses to various abiotic stresses such as salinity, drought, cadmium, mercury, ultraviolet radiation, reactive oxygen species, abscisic acid, and hematin. Based on the relationship analysis between nitric oxide, CO, and hydrogen peroxide, we proposed HO1 may be a central repeater for cross talk among them in plants.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2014
• Tom: 36
• Numer: 03
• Opis fizyczny: p.581-588,fig.,ref.

Twórcy

autor

He H.

• College of Agronomy, Guangxi University, Nanning, 530004, China
• Cash Crops Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, 530007, China

autor

He H.

• College of Agronomy, Guangxi University, Nanning, 530004, China

Bibliografia

• Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2005) Involvement of heme oxygenase as antioxidant defense in soybean nodules. Free Radic Res 39:145–151
• Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2006) Haem oxygenase activity and oxidative stress signaling in soybean leaves. Plant Sci 170:339–346
• Balestrasse KB, Yannarelli GG, Noriega GO, Batlle A, Tomaro ML (2008) Heme oxygenase and catalase gene expression in nodules and roots of soybean plants subjected to cadmium stress. Biometals 21:433–441
• Baranano DE, Rao M, Ferris CD, Snyder SH (2002) Biliverdin reductase: a major physiologic cytoprotectant. Proc Natl Acad Sci USA 99:16093–16098
• Baudouin E, Frendo P, Le Gleuher M, Puppo A (2004) A Medicago sativa haem oxygenase gene is preferentially expressed in root nodules. J Exp Bot 55:43–47
• Cao Z, Xuan W, Liu Z, Li X, Zhao N, Xu P, Wang Z, Guan R, Shen W (2007) Carbon monoxide promotes lateral root formation in rapeseed. J Integr Plant Biol 49:1070–1079
• Cao ZY, Geng BB, Xu S, Xuan W, Nie H, Shen WB, Liang YC, Guan RZ (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 XY, Ding X, Xu S, Wang R, Xuan W, Cao ZY, Chen J, Wu HH, Ye MB, Shen WB (2009) Endogenous hydrogen peroxide plays a positive role in the upregulation of heme oxygenase and acclimation to oxidative stress in wheat seedling leaves. J Integr Plant Biol 51:951–960
• 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 31:1085–1091
• Cui W, Fu G, Wu H, Shen W (2011) Cadmium-induced heme oxygenase-1 gene expression is associated with the depletion of glutathione in the roots of Medicago sativa. Biometals 24:93–103
• Cui WT, Li L, Gao ZZ, Wu HH, Xie YJ, Shen WB (2012) Haem oxygenase-1 is involved in salicylic acid-induced alleviation of oxidative stress due to cadmium stress in Medicago sativa. J Exp Bot 63:5521–5534
• 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
• Emborg TJ, Walker JM, Noh B, Vierstra RD (2006) Multiple heme oxygenase family members contribute to the biosynthesis of the phytochrome chromophore in Arabidopsis. Plant Physiol 140:856–868
• Foresti R, Motterlini R (1999) The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic Res 31:459–475
• Fu GQ, Xu S, Xie YJ, Han B, Nie L, Shen WB, Wang R (2011a) Molecular cloning, characterization, and expression of an alfalfa (Medicago sativa L.) heme oxygenase-1 gene, MsHO1, which is pro-oxidants-regulated. Plant Physiol Biochem 49:792–799
• Fu GQ, Zhang LF, Cui WT, Wang YQ, Shen WB, Ren Y, Zheng TQ (2011b) 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
• Gisk B, Yasui Y, Kohchi T, Frankenberg-Dinkel N (2010) Characterization of the haem oxygenase protein family in Arabidopsis thaliana reveals a diversity of functions. Biochem J 425:425–434
• Gohya T, Zhang X, Yoshida T, Migita CT (2006) Spectroscopic characterization of a higher plant heme oxygenase isoform-1 from Glycine max (soybean): coordination structure of the heme complex and catabolism of heme. FEBS J 273:5384–5399
• 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
• Han Y, Xuan W, Yu T, Fang WB, Lou TL, Gao Y, Chen XY, Xiao X, Shen WB (2007) Exogenous hematin alleviates mercury-induced oxidative damage in the roots of Medicago sativa. J Integr Plant Biol 49:1703–1713
• Han Y, Zhang J, Chen XY, Gao ZZ, Xuan W, Xu S, Ding X, Shen WB (2008) Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. New Phytol 177:155–166
• Hsu YY, Chao YY, Kao CH (2013) Methyl jasmonate-induced lateral root formation in rice: the role of heme oxygenase and calcium. J Plant Physiol 170:63–69
• Huang BK, Xu S, Xuan W, Li M, Cao ZY, Liu KL, Ling TF, Shen WB (2006) Carbon monoxide alleviates salt-induced oxidative damage in wheat seedling leaves. J Integr Plant Biol 48:249–254
• Huang JJ, Han B, Xu S, Zhou MX, Shen WB (2010) 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
• Izawa T, Qikawa T, Tokutomi S, Okuno K, Shimamoto K (2000) Phytochromes confer the photoperiodic control of flowering in rice (a short-day plant). Plant J 22:391–399
• Jin QJ, Zhu KK, Xie YJ, Shen WB (2013) Heme oxygenase-1 is involved in ascorbic acid-induced alleviation of cadmium toxicity in root tissues of Medicago sativa. Plant Soil 366: 605–616
• Kao CH (2013) Role of rice heme oxygenase in lateral root formation. Plant Signal Behav 8:e25766
• Keyse SM, Tyrrell RMm (1989) Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 86:99–103
• Ling T, Zhang B, Cui W, Wu M, Lin J, Zhou W, Huang J, Shen WB (2009) Carbon monoxide mitigates salt-induced inhibition of root growth and suppresses programmed cell death in wheat primary roots by inhibiting superoxide anion overproduction. Plant Sci 177:331–340
• Liu KL, Xu S, Xuan W, Ling TF, Cao ZY, Huang BK, Sun YG, Fang L, Liu ZY, Zhao N, Shen WB (2007) Carbon monoxide counteracts the inhibition of seed germination and alleviates oxidative damage caused by salt stress in Oryza sativa. Plant Sci 172:544–555
• 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
• Maines MD (1997) The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37: 517–554
• Motterlini R, Foresti R, Bassi R, Calabrese V, Clark JE, Green CJ (2000) Endothelial haem oxygenase-1 induction by hypoxia. Modulation by inducible nitric oxide synthase and S-nitrosothiols. J Biol Chem 275:13613–13620
• 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 haem oxygenase. Plant Cell 11:335–347
• Muramoto T, Tsurui N, Terry MJ, Yokota A, Kohchi T (2002) Expression and biochemical properties of a ferredoxin-dependent heme oxygenase required for phytochrome chromophore synthesis. Plant Physiol 130:1958–1966
• Nath KA, Balla G, Vercellotti G, Balla J, Jacob HS, Levitt MD, Rosenberg ME (1992) Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 90:267–270
• 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
• Noriega GO, Yannarelli GG, Balestrasse KB, Batlle A, Tomaro ML (2007) The effect of nitric oxide on heme oxygenase gene expression in soybean leaves. Planta 226:1155–1163
• Ryter SW, Otterbein LE, Morse D, Choi AMK (2002) Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem 234(235): 249–263
• Santa-Cruz DM, Pacienza NA, Polizio AH, Balestrasse KB, Tomaro ML, Yannarelli GG (2010) Nitric oxide synthase like dependent NO production enhances heme oxygenase up-regulation in ultraviolet-B-irradiated soybean plants. Phytochemistry 71: 1700–1707
• Stocker R, Yamamoto Y, Mc Donagh AF, Glazer AN, Ames BN (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235:1043–1046
• Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61:748–755
• Wei MY, Chao YY, Kao CH (2013) NaCl-induced heme oxygenase in roots of rice seedlings is mediated through hydrogen peroxide. Plant Growth Regul 69:209–214
• Wu M, Huang J, Xu S, Ling T, Xie Y, Shen W (2011) Haem oxygenase delays programmed cell death in wheat aleurone layers by modulation of hydrogen peroxide metabolism. J Exp Bot 62:235–248
• Wu MZ, Wang FQ, Zhang C, Xie YJ, Han B, Huang JJ, Shen WB (2013) Heme oxygenase-1 is involved in nitric oxide- and cGMP-induced α-Amy2/54 gene expression in GA-treated wheat aleurone layers. Plant Mol Biol 81:27–40
• Xie YJ, Ling TF, Han Y, Liu KL, Zheng QS, Huang LQ, Yuan XX, He Z, 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 defense in wheat seedling root. Plant Cell Environ 31:1864–1881
• Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292
• Xu S, Zhang B, Cao ZY, Ling TF, Shen WB (2010a) Heme oxygenase is involved in cobalt chloride-induced lateral root development in tomato. Biometals 24:181–191
• Xu S, Lou TL, Zhao N, Gao Y, Dong LH, Jiang RJ, Shen WB, Huang LQ, Wang R (2010b) 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
• 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
• Yu CZ, Benkai H, Ya WQ, Wei X, Fang LT, Bo Z, Xi C, Li N, WenBiao S (2007) Involvement of carbon monoxide produced by heme oxygenase in ABA induced stomatal closure in Vicia faba and its proposed signal transduction pathway. Chin Sci Bull 52:2365–2373
• Zilli CG, Balestrasse KB, Yannarelli GG, Polizio AH, Santa-Cruz DM, Tomaro ML (2008) Heme oxygenase up-regulation under salt stress protects nitrogen metabolism in nodules of soybean plants. Environ Exp Bot 64:83–89

Identyfikatory

DOI

10.1007/s11738-013-1444-1