Heme oxygenase-1 is involved in sodium hydrosulfide-induced lateral root formation in tomato seedlings

Plant Cell Reports

Volumn 33, Issue 6, 2014, Pages 969-978

  Fang, Tao ^a   Li, Jiale ^a   Cao, Zeyu ^a   Chen, Meng ^a   Shen, Wei ^a   Huang, Liqin ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Cell cycle regulatory genes; Heme oxygenase 1; Hydrogen sulfide; Lateral root formation; Sodium hydrosulfide; Solanum lycopersicum

Indexed keywords

CARBON MONOXIDE; CELL CYCLE PROTEIN; HEME OXYGENASE 1; HEMIN; HYDROGEN SULFIDE; SODIUM BISULFIDE; SULFIDE; VEGETABLE PROTEIN;

BIOLOGICAL MODEL; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT ROOT; SEEDLING; TOMATO;

CARBON MONOXIDE; CELL CYCLE PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HEME OXYGENASE-1; HEMIN; HYDROGEN SULFIDE; LYCOPERSICON ESCULENTUM; MODELS, BIOLOGICAL; PLANT PROTEINS; PLANT ROOTS; SEEDLING; SULFIDES;

EID: 84900843565     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-014-1577-8     Document Type: Article

References (59)

1. Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16: 1066-1071.
2. Akamatsu Y, Haga M, Tyagi S, Yamashita K, Graça-Souza AV, Ollinger R, Czismadia E, May GA, Ifedigbo E, Otterbein LE, Bach FH, Soares MP (2004) Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J 18: 771-772.
3. Blakely LM, Blakely RM, Colowit PM, Elliott DS (1988) Experimental studies on lateral root formation in radish seedling roots: II. Analysis of the dose-response to exogenous auxin. Plant Physiol 87: 414-419.
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
5. Burssens S, Himanen K, van de Cotte B, Beeckman T, van Montagu M, Inzé D, Verbruggen N (2000) Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211: 632-640.
6. 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: 1070-1079.
7. 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.
8. Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inzé D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13: 843-852.
9. 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.
10. 2-induced lateral root formation in apocynin-treated rice. Plant Cell Rep 32: 219-226.
11. Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70: 278-286.
12. Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57: 581-588.
13. Cui W, Li L, Gao Z, Wu H, Xie Y, Shen W (2012a) 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.
14. Cui WT, Liu RT, Lin YT, Xie YJ, Shen WB (2012b) Carbon monoxide: a new member of the gaseous signalling molecule in plants. J Nanjing Agric Univ 35: 87-92.
15. Cui W, Zhang J, Xuan W, Xie Y (2013) Up-regulation of heme oxygenase-1 contributes to the amelioration of aluminum-induced oxidative stress in Medicago sativa. J Plant Physiol 170: 1328-1336.
16. D'Araio E, Shaw N, Millward A, Demaine A, Whiteman M, Hodgkinson A (2014) Hydrogen sulfide induces heme oxygenase-1 in human kidney cells. Acta Diabetol. doi: 10. 1007/s00592-013-0501-y.
17. 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.
18. De Veylder L, Beeckman T, Inzé D (2007) The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 8: 655-665.
19. García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188: 977-984.
20. 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.
21. Hosoki R, Matsuki N, Kimura H (1997) The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237: 527-531.
22. Jeong GS, Oh GS, Pae HO, Jeong SO, Kim YC, Shin MK, Seo BY, Han SY, Lee HS, Jeong JG, Koh JS, Chung HT (2006) Comparative effects of curcuminoids on endothelial heme oxygenase-1 expression: ortho-methoxy groups are essential to enhance heme oxygenase activity and protection. Exp Mol Med 38: 393-400.
23. Jin QJ, Yuan XX, Cui WT, Han B, Feng JF, Xu S, Shen WB (2012) Isolation and characterization of a heme oxygenase-1 gene from Chinese cabbage. Mol Biotechnol 50: 8-17.
24. Jin Q, Zhu K, Cui W, Xie Y, Han B, Shen W (2013a) Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquat-induced oxidative stress via the modulation of heme oxygenase-1 signalling system. Plant Cell Environ 36: 956-969.
25. Jin QJ, Zhu KK, Xie YJ, Shen WB (2013b) Heme oxygenase-1 is involved in ascorbic acid-induced alleviation of cadmium toxicity in root tissues of Medicago sativa. Plant Soil 366: 605-616.
26. Lee HW, Kim NY, Lee DJ, Kim J (2009) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiol 151: 1377-1389.
27. Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51: 169-187.
28. Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25: 617-631.
29. Liao YF, Zhu W, Li DP, Zhu X (2013) Heme oxygenase-1 and gut ischemia/reperfusion injury: a short review. World J Gastroenterol 19: 3555-3561.
30. 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 31: 519-528.
31. Lin Y, Zhang W, Qi F, Cui W, Xie Y, Shen W (2014) Hydrogen-rich water regulates cucumber adventitious root development in a heme oxygenase-1/carbon monoxide-dependent manner. J Plant Physiol 171: 1-8.
32. Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36: 1607-1616.
33. Motterlini R, Green CJ, Foresti R (2002) Regulation of heme oxygenase-1 by redox signals involving nitric oxide. Antioxid Redox Signal 4: 615-624.
34. 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.
35. 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.
36. 2S toxicity in erythrocytes from a marine invertebrate. J Exp Biol 211: 3816-3825.
37. Péret B, De Rybel B, Casimiro I, Benková E, Swaru R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14: 399-408.
38. Ryter SW, Otterbein LE, Morse D, Choi AM (2002) Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem 234-235: 249-263.
39. Sauter M, Wiegen PV, Lörz H, Kranz E (1998) Cell cycle regulatory genes from maize are differentially controlled during fertilization and first embryonic cell division. Sex Plant Reprod 11: 41-48.
40. Shekhawat GS, Verma K (2010) Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. J Exp Bot 61: 2255-2270.
41. Su GX, Zhang WH, Liu YL (2006) Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. J Integr Plant Biol 48: 426-432.
42. Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65: 67-74.
43. Taylor BH, Scheuring CF (1994) A molecular marker for lateral root initiation: the RSI-1 gene of tomato (Lycopersicon esculentum Mill) is activated in early lateral root primordia. Mol Gen Genet 243: 148-157.
44. Terry MJ, Kendrick RE (1996) The aurea and yellow-green-2 mutants of tomato are deficient in phytochrome chromophore synthesis. J Biol Chem 271: 21681-21686.
45. Verkest A, Weinl C, Inzé D, De Veylder L, Schnittger A (2005) Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiol 139: 1099-1106.
46. Wang R (2003) The gasotransmitter role of hydrogen sulfide. Antioxid Redox Signal 5: 493-501.
47. 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.
48. 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.
49. Wu J, Wang F, Cheng L, Kong F, Peng Z, Liu S, Yu X, Lu G (2011) Identification, isolation and expression analysis of auxin response factor (ARF) genes in Solanum lycopersicum. Plant Cell Rep 30: 2059-2073.
50. Wu M, Wang F, Zhang C, Xie Y, Han B, Huang J, Shen W (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.
51. Xie Y, Lai D, Mao Y, Zhang W, Shen W, Guan R (2013a) Molecular cloning, characterization, and expression analysis of a novel gene encoding l-cysteine desulfhydrase from Brassica napus. Mol Biotechnol 54: 737-746.
52. Xie Y, Mao Y, Lai D, Zhang W, Zheng T, Shen W (2013b) Roles of NIA/NR/NOA1-dependent nitric oxide production and HY1 expression in the modulation of Arabidopsis salt tolerance. J Exp Bot 64: 3045-3060.
53. Xu S, Zhang B, Cao ZY, Ling TF, Shen WB (2011) Heme oxygenase is involved in cobalt chloride-induced lateral root development in tomato. Biometals 24: 181-191.
54. 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.
55. Xuan W, Xu S, Li M, Han B, Zhang B, Zhang J, Lin Y, Huang J, Shen W, Cui J (2012) Nitric oxide is involved in hemin-induced cucumber adventitious rooting process. J Plant Physiol 169: 1032-1039.
56. Yannarelli GG, Gallego SM, Tomaro ML (2006) Effect of UV-B radiation on the activity and isoforms of enzymes with peroxidase activity in sunflower cotyledons. Environ Exp Bot 56: 174-181.
57. Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51: 1086-1094.
58. Zhang H, Jiao H, Jiang CX, Wang SH, Wei ZJ, Luo JP, Jones RL (2010) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 32: 849-857.
59. Zhang C, Li Y, Yuan F, Hu S, He P (2012) Effects of hematin and carbon monoxide on the salinity stress responses of Cassia obtusifolia L. seeds and seedlings. Plant Soil 359: 85-105.