Increased expression of Fe-chelatase leads to increased metabolic flux into heme and confers protection against photodynamically induced oxidative stress
详细信息    查看全文
  • 作者:Jin-Gil Kim (1)
    Kyoungwhan Back (2)
    Hyoung Yool Lee (2)
    Hye-Jung Lee (3)
    Thu-Ha Phung (1)
    Bernhard Grimm (3)
    Sunyo Jung (1)
  • 关键词:Fe ; chelatase ; Heme ; Oxidative stress resistance ; Porphyrin ; Transgenic rice
  • 刊名:Plant Molecular Biology
  • 出版年:2014
  • 出版时间:October 2014
  • 年:2014
  • 卷:86
  • 期:3
  • 页码:271-287
  • 全文大小:1,207 KB
  • 参考文献:1. Alawady AE, Grimm B (2005) Tobacco Mg protoporphyrin IX methyltransferase is involved in inverse activation of Mg porphyrin and protoheme synthesis. Plant J 41:282鈥?90 CrossRef
    2. Asada K (1994) Production and action of active oxygen species in photosynthetic tissues. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defence systems in plants. CRC Press, Boca Raton, pp 77鈥?04
    3. Avin-Wittenberg T, Tzin V, Angelovici R, Less H, Galili G (2012) Deciphering energy-associated gene networks operating in the response of Arabidopsis plants to stress and nutritional cues. Plant J 70:954鈥?66 CrossRef
    4. Barajas-L蠈pez JD, Blanco NE, Strand A (2013) Plastid-to-nucleus communication, signals controlling the running of the plant cell. Biochim Biophys Acta 1833:425鈥?37 CrossRef
    5. Beale SI, Weinstein JD (1990) Tetrapyrrole metabolism in photosynthetic organisms. In: Dailey HA (ed) Biosynthesis of heme and chlorophylls. McGraw-Hill, New York, pp 287鈥?91
    6. Buege TA, Aust SD (1978) Microsomal lipid peroxidation. Method Enzymol 52:302鈥?10 CrossRef
    7. Chi W, Sun X, Zhang L (2013) Intracellular signaling from plastid to nucleus. Annu Rev Plant Biol 64:559鈥?82 CrossRef
    8. Chow KS, Singh DP, Roper JM, Smith AG (1997) A single precursor protein for ferrochelatase-I from / Arabidopsis is imported / in / vitro into both chloroplasts and mitochondria. J Biol Chem 272:27565鈥?7571 CrossRef
    9. Cleary SP, Tan FC, Nakrieko K-A, Thompson SJ, Mullineaux PM, Creissen GP, von Stedingk E, Glaser E, Smith AG, Robinson C (2002) Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. J Biol Chem 277:5562鈥?569 CrossRef
    10. Cornah JE, Roper JM, Singh DP, Smith AG (2002) Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and nonphotosynthetic cells of pea ( / Pisum sativum L.). Biochem J 362:423鈥?32 CrossRef
    11. Dayan FE, Rimando AM, Duke SO, Jacobs NJ (1999) Thiol-dependent degradation of protoporphyrin IX by plant peroxidases. FEBS Lett 444:227鈥?30 CrossRef
    12. Franklin KA, Linley PJ, Montgomery BL, Lagarias JC, Thomas B, Jackson SD, Terry MJ (2003) Misregulation of tetrapyrrole biosynthesis in transgenic tobacco seedlings expressing mammalian biliverdin reductase. Plant J 35:717鈥?28 CrossRef
    13. 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鈥?34 CrossRef
    14. Ha SB, Lee SB, Lee Y, Yang K, Lee N, Jang SM, Chung JS, Jung S, Kim YS, Wi SG, Back K (2004) The plastidic / Arabidopsis protoporphyrinogen IX oxidase gene, with or without the transit sequence, confers resistance to the diphenyl ether herbicide in rice. Plant Cell Environ 27:79鈥?8 CrossRef
    15. Hansson A, Kannangara CG, von Wettstein D, Hansson M (1999) Molecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase. Proc Natl Acad Sci USA 96:1744鈥?749 CrossRef
    16. Haworth P, Hess FD (1988) The generation of singlet oxygen (1O2) by the nitrodiphenyl ether herbicide oxyfluorfen is independent of photosynthesis. Plant Physiol 86:672鈥?76 CrossRef
    17. Jung S, Lee Y, Yang K, Lee SB, Jang SM, Ha SB, Back K (2004) Dual targeting of / Myxococcus xanthus protoporphyrinogen oxidase into chloroplasts and mitochondria and high level oxyfluorfen resistance. Plant Cell Environ 27:1436鈥?446 CrossRef
    18. Jung S, Lee H-J, Lee Y, Kang K, Kim YS, Grimm B, Back K (2008) Toxic tetrapyrrole accumulation in protoporphyrinogen IX oxidase-overexpressing transgenic rice plants. Plant Mol Biol 67:535鈥?46 CrossRef
    19. Kang K, Lee K, Park S, Lee S, Kim YS, Back K (2010) Overexpression of rice ferrochelatase I and II leads to increased susceptibility to oxyfluorfen herbicide in transgenic rice. J Plant Biol 53:291鈥?96 CrossRef
    20. Kindgren P, Eriksson M-J, Benedict C, Mohapatra A, Gough SP, Hansson M, Kieselbach T, Strand 脜 (2011) A novel proteomic approach reveals a role for Mg鈥損rotoporphyrin IX in response to oxidative stress. Physiol Plant 141:310鈥?20 CrossRef
    21. Koch M, Breithaupt C, Kiefersauer R, Greigang J, Huber R, Messerschmidt A (2004) Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J 23:1720鈥?728 CrossRef
    22. Lee HJ, Duke SO (1994) Protoporphyrinogen IX-oxidizing activities involved in the mode of action of peroxidizing herbicides. J Agric Food Chem 42:2610鈥?618 CrossRef
    23. Lee HJ, Ball MD, Parham R, Rebeiz CA (1992) Chloroplast biogenesis 65: enzymic conversion of protoporphyrin IX to Mg-protoporphyrin IX in a subplastidic membrane fraction of cucumber etiochloroplasts. Plant Physiol 99:1134鈥?140 CrossRef
    24. Lee HJ, Duke MV, Birk JH, Yamamoto M, Duke SO (1995) Biochemical and physiological effects of benzheterocycles and related compounds. J Agric Food Chem 43:2722鈥?727 CrossRef
    25. Lee HJ, Lee SB, Chung JS, Han SU, Han O, Guh JO, Jeon JS, An G, Back K (2000) Transgenic rice plants expressing a / Bacillus subtilis protoporphyrinogen oxidase gene are resistant to diphenyl ether herbicide oxyfluorfen. Plant Cell Physiol 41:743鈥?49 CrossRef
    26. Lermontova I, Grimm B (2000) Overexpression of plastidic protoporphyrinogen IX oxidase leads to resistance to the diphenyl-ether herbicide acifluorfen. Plant Physiol 122:75鈥?3 CrossRef
    27. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350鈥?82 CrossRef
    28. Lister R, Chew O, Rudhe C, Lee MN, Whelan J (2001) / Arabidopsis thaliana ferrochelatase-I and -II are not imported into / Arabidopsis mitochondria. FEBS Lett 506:291鈥?95 CrossRef
    29. Masuda T, Suzuki T, Shimada H, Ohta H, Takamiya K (2003) Subcellular localization of two types of ferrochelatase in cucumber. Planta 217:602鈥?09 CrossRef
    30. Matringe M, Scalla R (1988) Studies on the mode of action of acifluorfen-methyl in non-chlorophyllous cells: accumulation of tetrapyrroles. Plant Physiol 86:619鈥?22 CrossRef
    31. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis / genomes uncoupled 5 ( / GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98:2053鈥?058 CrossRef
    32. Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A (2008) The steady state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in / Arabidopsis. Proc Natl Acad Sci USA 105:15184鈥?5189 CrossRef
    33. Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M, Smith AG, Tanaka A, Terry MJ (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 15:488鈥?98 CrossRef
    34. M枚ller SG, Kundel T, Chua N-H (2001) A plastidic ABC protein involved in intercompartmental communication of light signaling. Genes & Dev 15:90鈥?03 CrossRef
    35. Moore MR (1993) Biochemistry of porphyria. Int J Biochem 25:1353鈥?368 CrossRef
    36. Moulin M, McCormac AC, Terry MJ, Smith AG (2008) Tetrapyrrole profiling in / Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci USA 105:15178鈥?5183 CrossRef
    37. 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鈥?966 CrossRef
    38. Nagai S, Koide M, Takahashi S, Kikuta A, Mitsuko A, Sasaki-Sekimoto Y, Ohta H, Takamiya K-I, Masuda T (2007) Induction of isoforms of tetrapyrrole biosynthetic enzymes, / AtHEMA2 and / AtFC1, under stress conditions and their physiological functions in / Arabidopsis. Plant Physiol 144:1039鈥?051 CrossRef
    39. Nordmann Y, Deybach J-C (1990) Human hereditary porphyries. In: Dailey HA (ed) Biosynthesis of Heme and Chlorophylls. McGraw-Hill, New York, pp 491鈥?42
    40. 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鈥?008 CrossRef
    41. Olson PD, Varner JE (1993) Hydrogen peroxide and lignification. Plant J 4:887鈥?92 CrossRef
    42. Otterbein LE, Soares MP, Yamashita K, Bach FH (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449鈥?55 CrossRef
    43. Papenbrock J, Grimm B (2001) Regulatory network of tetrapyrrole biosynthesis鈥攕tudies of intracellular signaling involved in metabolic and developmental control of plastids. Planta 213:667鈥?81 CrossRef
    44. Papenbrock J, Mock HP, Kruse E, Grimm B (1999) Expression studies in tetrapyrrole biosynthesis: inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods. Planta 208:264鈥?73 CrossRef
    45. Papenbrock J, Mock H-P, Pf眉ndel E, Grimm B (2000) Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. Plant J 22:155鈥?64 CrossRef
    46. Papenbrock J, Mishra S, Mock HP, Kruse E, Schmidt EK, Petersmann A, Braun HP, Grimm B (2001) Impaired expression of the plastidic ferrochelatase by antisense RNA synthesis leads to a necrotic phenotype of transformed tobacco plants. Plant J 28:41鈥?0 CrossRef
    47. Peter E, Rothbart M, Oelze M-L, Shalygo N, Dietz K-J, Grimm B (2010) Mg protoporphyrin monomethylester cyclase deficiency and effects on tetrapyrrole metabolism in different light conditions. Plant Cell Physiol 51:1229鈥?241 CrossRef
    48. Phung T-H, Jung H-I, Park J-H, Kim J-G, Back K, Jung S (2011) Porphyrin biosynthesis control under water stress: sustained porphyrin status correlates with drought tolerance in transgenic rice. Plant Physiol 157:1746鈥?764 CrossRef
    49. Pontier D, Albrieux C, Joyard J, Lagrange T, Block MA (2007) Knock-out of the magnesium protoporphyrin IX methyltransferase gene in Arabidopsis. Effects on chloroplast development and on chloroplast-to-nucleus signaling. J Biol Chem 282:2297鈥?304 CrossRef
    50. Pontoppidan B, Kannangara CG (1994) Purification and partial characterization of barley glutamyl-tRNA (Glu) reductase, the enzyme that directs glutamate to chlorophyll biosynthesis. Eur J Biochem 225:529鈥?37 CrossRef
    51. Porra RJ, Lascelles J (1968) Studies on ferrochelatase: the enzymatic formation of haem in proplastids, chloroplasts and plant mitochondria. Biochem J 108:343鈥?48
    52. Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of / Arabidopsis thaliana. Plant Physiol 110:125鈥?36 CrossRef
    53. Ricchelli F (1995) Photophysical properties of porphyins in biological membranes. J Photochem Photobiol B Biol 29:109鈥?18 CrossRef
    54. Roper JM, Smith AG (1997) Molecular localization of ferrochelatase in higher plant chloroplasts. Eur J Biochem 246:32鈥?7 CrossRef
    55. Sassa S, Nagai T (1996) The role of heme in gene expression. Int J Hematol 63:167鈥?78 CrossRef
    56. Schneegurt MA, Beale SI (1986) Biosynthesis of protoheme and heme / a from glutamate in maize. Plant Physiol 81:965鈥?71 CrossRef
    57. Singh DP, Cornah JE, Hadingham S, Smith AG (2002) Expression analysis of the two ferrochelatase genes in / Arabidopsis in different tissues and under stress conditions reveals their different roles in haem biosynthesis. Plant Mol Biol 50:773鈥?88 CrossRef
    58. Smith AG (1988) Subcellular localization of two porphyrin-synthesis enzymes in / Pisum sativum (pea) and / Arum (cuckoo-pint) species. Biochem J 249:423鈥?28
    59. Smith AG, Marsh O, Elder GH (1993) Investigation of the subcellular location of the tetrapyrrole-biosynthesis enzyme coprotoporphyrinogen oxidase in higher plants. Biochem J 292:503鈥?08
    60. Soldatova O, Apchelimov A, Radukina N, Ezhova T, Shestakov S, Ziemann V, Hedtke B, Grimm B (2005) An / Arabidopsis mutant that is resistant to the protoporphyrinogen oxidase inhibitor acifluorfen shows regulatory changes in tetrapyrrole biosynthesis. Mol Gen Genomics 273:311鈥?18 CrossRef
    61. Srivastava A, Beale SI (2005) Glutamyl-tRNA reductase of / Chlorobium vibrioforme is a dissociable homodimer that contains one tightly bound heme per subunit. J Bacteriol 187:4444鈥?450 CrossRef
    62. Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421:79鈥?3 CrossRef
    63. Suzuki T, Masuda T, Singh DP, Tan FC, Tsuchiya T, Shimada H, Ohta H, Smith AG, Takamiya K (2002) Two types of ferrochelatase in photosynthetic and nonphotosynthetic tissues of cucumber: their difference in phylogeny, gene expression, and localization. J Biol Chem 277:4731鈥?737 CrossRef
    64. Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248鈥?55 CrossRef
    65. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321鈥?46 CrossRef
    66. Terry MJ, Smith AG (2013) A model for tetrapyrrole synthesis as the primary mechanism for plastid-to-nucleus signaling during chloroplast biogenesis. Front Plant Sci 4:14 CrossRef
    67. Terry MJ, Linley PJ, Kohchi T (2002) Making light of it: the role of plant heme oxygenases in phytochrome chromophore synthesis. Biochem Soc Trans 30:604鈥?09 CrossRef
    68. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley鈥損owdery mildew interaction. Plant J 11:1187鈥?194 CrossRef
    69. Ujwal ML, McCormac AC, Goulding A, Kumar AM, Soll D, Terry MJ (2002) Divergent regulation of the / HEMA gene family encoding glutamyl-tRNA reductase in / Arabidopsis thaliana: expression of / HEMA2 is regulated by sugars, but is independent of light and plastid signaling. Plant Mol Biol 50:83鈥?1 CrossRef
    70. Vanhee C, Batoko H (2011) Arabidopsis TSPO and porphyrins metabolism. A transient signaling connection? Plant Signal Behav 6:1383鈥?385 CrossRef
    71. Vanhee C, Zapotoczny G, Masquelier D, Ghislain M, Batoko H (2011) The / Arabidopsis multistress regulator TSPO is a heme binding membrane protein and a potential scavenger of porphyrins via an autophagy-dependent degradation mechanism. Plant Cell 23:785鈥?05 CrossRef
    72. Vasileuskaya Z, Oster U, Beck CF (2005) Mg-protoporphyrin IX and heme control / HEMA, the gene encoding the first specific step of tetrapyrrole biosynthesis, in / Chlamydomonas reinhardtii. Eukaryot Cell 4:1620鈥?628 CrossRef
    73. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949鈥?56 CrossRef
    74. von Gromoff ED, Alawady A, Meinecke L, Grimm B, Beck CF (2008) Heme, a plastid-derived regulator of nuclear gene expression in / Chlamydomonas. Plant cell 20:552鈥?67 CrossRef
    75. Vothknecht UC, Kannangara CG, von Wettstein D (1998) Barley glutamyl tRNAGlu reductase: mutations affecting haem inhibition and enzyme activity. Phytochemistry 47:513鈥?19 CrossRef
    76. Vo脽 B, Meinecke L, Kurz T, Al-Babili S, Beck CF, Hess WR (2011) Hemin and magnesium-protoporphyrin IX induce global changes in gene expression in / Chlamydomonas reinhardtii. Plant Physiol 155:892鈥?05 CrossRef
    77. Woodbury W, Spencer AK, Stahman MA (1971) An improved procedure for using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301鈥?05 CrossRef
    78. Woodson JD, Perez-Ruiz JM, Chory J (2011) Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Cur Biol 21:897鈥?03 CrossRef
    79. 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鈥?162 CrossRef
    80. Zhang L, Hach A (1999) Molecular mechanism of heme signaling in yeast: the transcriptional activator Hap1 serves as the key mediator. Cell Mol Life Sci 56:415鈥?26 CrossRef
  • 作者单位:Jin-Gil Kim (1)
    Kyoungwhan Back (2)
    Hyoung Yool Lee (2)
    Hye-Jung Lee (3)
    Thu-Ha Phung (1)
    Bernhard Grimm (3)
    Sunyo Jung (1)

    1. School of Life Sciences and Biotechnology, Kyungpook National University, Daegu, 702-701, Korea
    2. Department of Biotechnology, Chonnam National University, Gwangju, 500-757, Korea
    3. Institute of Biology/Plant Physiology, Humboldt University, Philippstrasse 13, Building 12, 10115, Berlin, Germany
  • ISSN:1573-5028
文摘
Fe-chelatase (FeCh, EC 4.99.1.1) inserts Fe2+ into protoporphyrin IX (Proto IX) to form heme, which influences the flux through the tetrapyrrole biosynthetic pathway as well as fundamental cellular processes. In transgenic rice (Oryza sativa), the ectopic expression of Bradyrhizobium japonicum FeCh protein in cytosol results in a substantial increase of FeCh activity compared to wild-type (WT) rice and an increasing level of heme. Interestingly, the transgenic rice plants showed resistance to oxidative stress caused not only by the peroxidizing herbicide acifluorfen (AF) as indicated by a reduced formation of leaf necrosis, a lower conductivity, lower malondialdehyde and H2O2 contents as well as sustained Fv/Fm compared to WT plants, but also by norflurazon, paraquat, salt, and polyethylene glycol. Moreover, the transgenic plants responded to AF treatment with markedly increasing FeCh activity. The accompanying increases in heme content and heme oxygenase activity demonstrate that increased heme metabolism attenuates effects of oxidative stress caused by accumulating porphyrins. These findings suggest that increases in heme levels and porphyrin scavenging capacity support a detoxification mechanism serving against porphyrin-induced oxidative stress. This study also implicates heme as possibly being a positive signal in plant stress responses.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700