Stress signaling in response to polycyclic aromatic hydrocarbon exposure in Arabidopsis thaliana involves a nucleoside diphosphate kinase, NDPK-3

详细信息    查看全文

• 作者：Hong Liu (1)
  David Weisman (2)
  Ling Tang (3)
  Long Tan (1)
  Wen-ke Zhang (3)
  Zong-hua Wang (3)
  Yan-he Huang (1)
  Wen-xiong Lin (3)
  Xuan-ming Liu (4)
  Ad谩n Col贸n-Carmona (2)
  
  1. College of Resources and Environment ; Fujian Agriculture and Forestry University ; Fuzhou ; 350002 ; China
  2. Department of Biology ; University of Massachusetts ; 100 Morrissey Blvd ; Boston ; MA ; 02125-3393 ; USA
  3. The School of Life Sciences ; Fujian Agriculture and Forestry University ; Fuzhou ; 350002 ; China
  4. Department of Life Science ; College of Biology ; Hunan University ; Changsha ; 410082 ; China
  
• 关键词：Abiotic stress ; Nucleoside diphosphate kinase ; 3 ; Plant ; Phenanthrene ; Positive regulator
• 刊名：Planta
• 出版年：2015
• 出版时间：January 2015
• 年：2015
• 卷：241
• 期：1
• 页码：95-107
• 全文大小：3,197 KB
• 参考文献：1. Alkio M, Tabuchi TM, Wang X, Col贸n-Carmona A (2005) Stress responses to polycyclic aromatic hydrocarbons in / Arabidopsis include growth inhibition and hypersensitive response-like symptoms. J Exp Bot 56:2983鈥?994 CrossRef
  2. Baek D, Nam J, Koo YD, Kim DH, Lee J, Jeong JC, Kwak SS, Chung WS, Lim CO, Bahk JD, Hong JC, Lee SY, Kawai-Yamada M, Uchimiya H, Yun DJ (2004) Bax-induced cell death of / Arabidopsis is meditated through reactive oxygen-dependent and -independent processes. Plant Mol Biol 56:15鈥?7 1007/s11103-004-3096-4" target="_blank" title="It opens in new window">CrossRef
  3. Baird WM, Hooven LA, Mahadevan B (2005) Carcinogenic polycyclic aromatic hydrocarbon鈥揇NA adducts and mechanism of action. Environ Mol Mutagen 45:106鈥?14 1002/em.20095" target="_blank" title="It opens in new window">CrossRef
  4. Bjellqvist B, Pasquali C, Ravier F, Sanchez JC, Hochstrasser D (1993) A nonlinear wide-range immobilized pH gradient for two-dimensional electrophoresis and its definition in a relevant pH scale. Electrophoresis 14:1357鈥?365 1002/elps.11501401209" target="_blank" title="It opens in new window">CrossRef
  5. Burritt DJ (2008) The polycyclic aromatic hydrocarbon phenanthrene causes oxidative stress and alters polyamine metabolism in the aquatic liverwort / Riccia fluitans L. Plant Cell Environ 31:1416鈥?431 CrossRef
  6. Chen P, Xie JY, Liang SP (2000) Identification of protein spots in silver-stained two-dimensional gels by MALDI-TOF mass peptide map analysis. Acta Biochem Biophys Sin 32:387鈥?91
  7. Choi G, Yi H, Lee J, Kwon YK, Soh MS, Shin B, Luka Z, Hahn TR, Song PS (1999) Phytochrome signalling is mediated through nucleoside diphosphate kinase 2. Nature 401:610鈥?13 CrossRef
  8. Clough SJ, Bent AF (1998) Floral dip: a simplified method for / Agrobacterium mediated transformation of / Arabidopsis thaliana. Plant J 16:735鈥?43 CrossRef
  9. Core Team R (2012) R: a language and environment for statistical computing. R Foundation Statistical Computing, Vienna. ISBN 3-900051-07-0
  10. Cou茅e I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449鈥?59 CrossRef
  11. Cunningham SD, Anderson TA, Schwab AP, Hsu F (1996) Phytoremediation of soils contaminated with organic pollutants. In: Sparks DL (ed) Advances in agronomy. vol 56 Academic Press, pp 55鈥?14
  12. Dixit P, Mukherjee PK, Sherkhane PD, Kale SP, Eapen S (2011) Enhanced tolerance and remediation of anthracene by transgenic tobacco plants expressing a fungal glutathione transferase gene. J Hazard Mater 192:270鈥?76
  13. Dooki AD, Mayer-Posner FJ, Askari H, Aa Zaiee, Salekdeh GH (2006) Proteomic responses of rice young panicles to salinity. Proteomics 6:6498鈥?507 1002/pmic.200600367" target="_blank" title="It opens in new window">CrossRef
  14. Du YY, Wang PC, Chen J, Song CP (2008) Comprehensive functional analysis of the catalase gene family in / Arabidopsis thaliana. J Integr Plant Biol 50:1318鈥?326 CrossRef
  15. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis tool kit for the agricultural community. Nucl Acids Res 38:W64鈥揥70 CrossRef
  16. Eapen S, D鈥橲ouza SF (2005) Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol Adv 23:97鈥?14 CrossRef
  17. Fernandez J, Gharahdaghi F, Mische SM (1998) Routine identification of proteins from sodium dodecyl sulfate鈥損olyacrylamide gel electrophoresis (SDS-PAGE) gels or polyvinyl difluoride membranes using matrix assisted laser desorption/ionization-time of flight-mass spectrometry (MALDI-TOF-MS). Electrophoresis 19:1036鈥?045 1002/elps.1150190619" target="_blank" title="It opens in new window">CrossRef
  18. Frick CM, Farrell RE, Germida JJ (1999) Assessment of phytoremediation as an in situ technique for cleaning oil-contaminated sites. Tech. rep., Department of Soil Science, University of Saskatchewan
  19. Fukamatsu Y, Yabe N, Hasunuma K (2003) / Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases. Plant Cell Physiol 44:982鈥?89 CrossRef
  20. Gharahdaghi F, Weinberg CR, Meagher DA, Imai BS, Mische SM (1999) Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 20:601鈥?05 1002/(SICI)1522-2683(19990301)20:3<601::AID-ELPS601>3.0.CO;2-6" target="_blank" title="It opens in new window">CrossRef
  21. Guo J (2006) Laboratory manual of plant physiology. Higher Education Press, Beijing, pp 210鈥?28
  22. Hajheidari M, Abdollahian-Noghabi M, Askari H, Heidari M, Sadeghian SY, Ober ES, Salekdeh GH (2005) Proteome analysis of sugar beet leaves under drought stress. Proteomics 5:950鈥?60 1002/pmic.200401101" target="_blank" title="It opens in new window">CrossRef
  23. Hammargren J, Salinas T, Mar茅chal-Drouard L, Knorpp C (2007a) The pea mitochondrial nucleoside diphosphate kinase cleaves DNA and RNA. FEBS Lett 581:3507鈥?511 CrossRef
  24. Hammargren J, Sundstr枚m J, Johansson M, Bergman P, Knorpp C (2007b) On the phylogeny, expression and targeting of plant nucleoside diphosphate kinases. Physiol Plant 129:79鈥?9 CrossRef
  25. Hammargren J, Rosenquist S, Jansson C, Knorpp C (2008) A novel connection between nucleotide and carbohydrate metabolism in mitochondria: sugar regulation of the / Arabidopsis nucleoside diphosphate kinase 3a gene. Plant Cell Rep 27:529鈥?34 1007/s00299-007-0486-5" target="_blank" title="It opens in new window">CrossRef
  26. Haque ME, Yoshida Y, Hasunuma K (2010) ROS resistance in / Pisum sativum cv. Alaska: the involvement of nucleoside diphosphate kinase in oxidative stress responses via the regulation of antioxidants. Planta 232:367鈥?82 1007/s00425-010-1173-2" target="_blank" title="It opens in new window">CrossRef
  27. Harvey PJ, Campanella BF, Castro PML, Harms H, Lichtfouse E, Sch盲ffner AR, Smrcek S, Werck-Reichhart D (2002) Phytoremediation of polyaromatic hydrocarbons, anilines and phenols. Environ Sci Pollut Res 9:29鈥?7 1007/BF02987315" target="_blank" title="It opens in new window">CrossRef
  28. Hasunuma K, Yoshida Y, Haque ME, Ny Wang, Fukamatsu Y, Miyoshi O, Lee B (2011) Global warming, plant paraquat resistance, and light signal transduction through nucleoside diphosphate kinase as a paradigm for increasing food supply. Naunyn-Schmiedebergs Arch Pharmacol 384:391鈥?95 1007/s00210-011-0640-z" target="_blank" title="It opens in new window">CrossRef
  29. Herberich E, Sikorski J, Hothorn T (2010) A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS One 5(3):e9788. doi:10.1371/journal.pone.0009788 CrossRef
  30. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346鈥?63 1002/bimj.200810425" target="_blank" title="It opens in new window">CrossRef
  31. Immel F, Renaut J, Masfaraud JF (2012) Physiological response and differential leaf proteome pattern in the European invasive Asteraceae / Solidago canadensis colonizing a former cokery soil. J Proteomics 75:1129鈥?143 CrossRef
  32. Kav NNV, Srivastava S, Goonewardene L, Blade SF (2004) Proteome-level changes in the roots of / Pisum sativum in response to salinity. Ann Appl Biol 145:217鈥?30 CrossRef
  33. Kim YH, Lim S, Yang KS, Kim CY, Kwon SY, Lee HS, Wang X, Zhou Z, Ma D, Yun DJ, Kwak SS (2009) Expression of / Arabidopsis / NDPK2 increases antioxidant enzyme activities and enhances tolerance to multiple environmental stresses in transgenic sweet potato plants. Mol Breed 24:233鈥?44 1007/s11032-009-9286-7" target="_blank" title="It opens in new window">CrossRef
  34. Kim MD, Kim YH, Kwon SY, Yun DJ, Kwak SS, Lee HS (2010) Enhanced tolerance to methyl viologen-induced oxidative stress and high temperature in transgenic potato plants overexpressing the / CuZnSOD, / APX and / NDPK2 genes. Physiol Plant 140:153鈥?62 CrossRef
  35. Kim YH, Kim MD, Choi YI, Park SC, Yun DJ, Noh EW, Lee HS, Kwak SS (2011) Transgenic poplar expressing / Arabidopsis / NDPK2 enhances growth as well as oxidative stress tolerance. Plant Biotech J 9:334鈥?47 CrossRef
  36. Knorpp C, Johansson M, Baird AM (2003) Plant mitochondrial nucleoside diphosphate kinase is attached to the membrane through interaction with the adenine nucleotide translocator. FEBS Lett 555:363鈥?66 CrossRef
  37. Kolb M, Harms H (2000) Metabolism of fluoranthene in different plant cell cultures and intact plants. Environ Toxicol Chem 19:1304鈥?310 1002/etc.5620190512" target="_blank" title="It opens in new window">CrossRef
  38. Kosov谩 K, V铆t谩mv谩s P, Pr谩拧il IT, Renaut J (2011) Plant proteome changes under abiotic stress鈥攃ontribution of proteomics studies to understanding plant stress response. J Proteomics 74:1301鈥?322 CrossRef
  39. Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of / Arabidopsis thaliana to stress combination. J Biol Chem 283:34197鈥?4203 CrossRef
  40. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940鈥?945 CrossRef
  41. Liao M, Li Y, Wang Z (2009) Identification of elicitor-responsive proteins in rice leaves by a proteomic approach. Proteomics 9:2809鈥?819 1002/pmic.200800192" target="_blank" title="It opens in new window">CrossRef
  42. Lima A, Farrington J, Reddy C (2005) Combustion-derived polycyclic aromatic hydrocarbons in the environment鈥攁 review. Environ Forensics 6:109鈥?31 CrossRef
  43. Liu H, Weisman D, Ye Y, Cui B, Huang Y, Col贸n-Carmona A, Wang Z (2009) An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in / Arabidopsis thaliana. Plant Sci 176:375鈥?82 CrossRef
  44. Ludwikow A, Gallois P, Sadowski J (2004) Ozone-induced oxidative stress response in / Arabidopsis: transcription profiling by microarray approach. Cell Mol Biol Lett 9:829鈥?42
  45. McClung CR (1997) Regulation of catalases in / Arabidopsis. Free Radical Biol Med 23:489鈥?96 CrossRef
  46. Moon H, Lee B, Choi G, Shin D, Prasad DT, Lee O, Kwak SS, Kim DH, Nam J, Bahk J, Hong JC, Lee SY, Cho MJ, Lim CO, Yun DJ (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 100:358鈥?63 CrossRef
  47. Nie L, Wu G, Culley DE, Scholten JCM, Zhang W (2007) Integrative analysis of transcriptomic and proteomic data: challenges, solutions and applications. Crit Rev Biotechnol 27:63鈥?5 CrossRef
  48. Paskova V, Hilscherova K, Feldmannova M, Blaha L (2006) Toxic effects and oxidative stress in higher plants exposed to polycyclic aromatic hydrocarbons and their N-heterocyclic derivatives. Environ Toxicol Chem 25:3238鈥?245 CrossRef
  49. Peng RH, Xu RR, Fu XY, Xiong AS, Zhao W, Tian YS, Zhu B, Jin XF, Chen C, Han HJ, Yao QH (2011) Microarray analysis of the phytoremediation and phytosensing of occupational toxicant naphthalene. J Hazard Mater 189:19鈥?6 CrossRef
  50. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:e45 CrossRef
  51. Phillips DH (1983) Fifty years of benzo(a)pyrene. Nature 303:468鈥?72 CrossRef
  52. Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15鈥?9 CrossRef
  53. 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
  54. Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in / Arabidopsis. J Biol Chem 279:11736鈥?1743 CrossRef
  55. Sams酶e-Petersen L, Larsen EH, Larsen PB, Bruun P (2002) Uptake of trace elements and PAHs by fruit and vegetables from contaminated soils. Environ Sci Technol 36:3057鈥?063 CrossRef
  56. Sweetlove LJ, Mowday B, Hebestreit HF, Leaver CJ, Millar AH (2001) Nucleoside diphosphate kinase III is localized to the inter-membrane space in plant mitochondria. FEBS Lett 508:272鈥?76 CrossRef
  57. Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on / Arabidopsis mitochondria. Plant J 32:891鈥?04 CrossRef
  58. Tang L, Kim MD, Yang KS, Kwon SY, Kim SH, Kim JS, Yun DJ, Kwak SS, Lee HS (2008) Enhanced tolerance of transgenic potato plants overexpressing / nucleoside diphosphate kinase 2 against multiple environmental stresses. Trans Res 17:705鈥?15 1007/s11248-007-9155-2" target="_blank" title="It opens in new window">CrossRef
  59. Tao S, Cui YH, Xu FL, Li BG, Cao J, Liu WX, Schmitt G, Wang XJ, Shen WR, Qing BP, Sun R (2004) Polycyclic aromatic hydrocarbons (PAHs) in agricultural soil and vegetables from Tianjin. Sci Total Environ 320:11鈥?4 CrossRef
  60. Valcu CM, Junqueira M, Shevchenko A, Schlink K (2009) Comparative proteomic analysis of responses to pathogen infection and wounding in / Fagus sylvatica. J Proteome Res 8:4077鈥?091 CrossRef
  61. vd Trenck T, Sandermann H (1980) Oxygenation of benzo[a]pyrene by plant microsomal fractions. FEBS Lett 119:227鈥?31 CrossRef
  62. vd Trenck T, Sandermann H (1981) Incorporation of benzo[alpha]pyrene quinones into lignin. FEBS Lett 125:72鈥?6 CrossRef
  63. Verslues PE, Batelli G, Grillo S, Agius F, Kim YS, Zhu J, Agarwal M, Katiyar-Agarwal S, Zhu JK (2007) Interaction of / SOS2 with nucleoside diphosphate kinase 2 and catalases reveals a point of connection between salt stress and H₂O₂ signaling in / Arabidopsis thaliana. Mol Cell Biol 27:7771鈥?780 CrossRef
  64. Wang X, Zhao H (2007) Uptake and biodegradation of polycyclic aromatic hydrocarbons by marine seaweed. J Coast Res Special 50:1056鈥?061
  65. Weigel D, Glazebrook J (2002) / Arabidopsis: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
  66. Weisman D, Alkio M, Col贸n-Carmona A (2010) Transcriptional responses to polycyclic aromatic hydrocarbon induced stress in / Arabidopsis thaliana reveal the involvement of hormone and defense signaling pathways. BMC Plant Biol 10:59 CrossRef
  67. Wild E, Dent J, Thomas GO, Jones KC (2005) Direct observation of organic contaminant uptake, storage, and metabolism within plant roots. Environ Sci Technol 39:3695鈥?702 CrossRef
  68. Yang KA, Moon H, Kim G, Lim CJ, Hong JC, Lim CO, Yun DJ (2003) / NDP kinase 2 regulates expression of antioxidant genes in / Arabidopsis. P Japan Acad B-Phys 79B:86鈥?1 CrossRef
  69. Yang YJ, Zuo ZC, Zhao XY, Li X, Klejnot J, Li Y, Chen P, Liang SP, Yu XH, Liu XM, Lin CT (2008) Blue-light-independent activity of / Arabidopsis cryptochromes in the regulation of steady-state levels of protein and mRNA expression. Mol Plant 1:167鈥?77 CrossRef
  70. Yoshida Y, Ogura Y, Hasunuma K (2006) Interaction of nucleoside diphosphate kinase and catalases for stress and light responses in neurospora crassa. FEBS Lett 580:3282鈥?286 CrossRef
  
• 刊物主题：Plant Sciences; Agriculture; Ecology; Forestry;
• 出版者：Springer Berlin Heidelberg
• ISSN：1432-2048

文摘

Main conclusion The study is the first to reveal the proteomic response in plants to a single PAH stress, and indicates that NDPK3 is a positive regulator in the Arabidopsis response to phenanthrene stress. Abstract Polycyclic aromatic hydrocarbons (PAHs) are highly carcinogenic pollutants that are byproducts of carbon-based fuel combustion, and tend to persist in the environment for long periods of time. PAHs elicit complex, damaging responses in plants, and prior research at the physiological, biochemical, and transcriptional levels has indicated that reactive oxygen species (ROS) and oxidative stress play major roles in the PAH response. However, the proteomic response has remained largely unexplored. This study hypothesized that the proteomic response in Arabidopsis thaliana to phenanthrene, a model PAH, would include a strong oxidative stress signature, and would provide leads to potential signaling molecules involved. To explore that proteomic signature, we performed 2D-PAGE experiments and identified 30 proteins levels that were significantly altered including catalases (CAT), ascorbate peroxidase (APX), peroxiredoxins (POD), glutathione-S-transferase, and glutathione reductase. Also upregulated was nucleoside diphosphate kinase 3 (NDPK-3), a protein known to have metabolic and stress signaling functions. To address whether NDPK-3 functions upstream of the oxidative stress response, we measured levels of stress-responsive enzymes in NDPK-3 overexpressor, loss-of-function knockout, and wild-type plant lines. In the NDPK-3 overexpressor, the enzyme activities of APX, CAT, POD, as well as superoxide dismutase were all increased compared to wild type; in the NDPK-3 knockout line, these enzymes had reduced activity. This pattern occurred in untreated as well as phenanthrene-treated plants. These data support a model in which NDPK-3 is a positive regulator of the Arabidopsis stress response to PAHs.