Abstract
Main Conclusion
Rice plants employ two strategies to cope with Cr toxicity: immobilizing Cr ions into cell walls to reduce its translocation and activating antioxidant defense to mitigate Cr-induced oxidative stress.
The investigation aimed at understanding the physiological and proteomic responses of rice seedlings to hexavalent chromium (Cr6+) stress was conducted using two rice genotypes, which differ in Cr tolerance and accumulation. Cr toxicity (200 µM) heavily increased the accumulation of H2O2 and \({\text{O}}_{2}^{{ \cdot-}}\), enhanced lipid peroxidation, decreased cell viability and consequently inhibited rice plant growth. Proteomic analyses suggest that the response of rice proteome to Cr stress is genotype- and Cr dosage-dependent and tissue specific. Sixty-four proteins, which show more than fourfold difference under either two Cr levels, have been successfully identified. They are involved in a range of cellular processes, including cell wall synthesis, energy production, primary metabolism, electron transport and detoxification. Two proteins related to cell wall structure, NAD-dependent epimerase/dehydratase and reversibly glycosylated polypeptide were greatly up-regulated by Cr stress. Their enhancements coupled with callose accumulation by Cr suggest that cell wall is an important barrier for rice plants to resist Cr stress. Some enzymes involved in antioxidant defense, such as ferredoxin-NADP reductase, NADP-isocitrate dehydrogenase, glyoxalase I (Gly I) and glutamine synthetase 1 (GS1) have also been identified in response to Cr stress. However, they were only detected in Cr-tolerant genotype, indicating the genotypic difference in the capacity of activating the defense system to fight against Cr-induced oxidative stress. Overall, two strategies in coping with Cr stress in rice plants can be hypothesized: (i) immobilizing Cr ions into cell walls to reduce its translocation and (ii) activating antioxidant defense to mitigate Cr-induced oxidative stress.
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Abbreviations
- 2-DE:
-
Two-dimensional gel electrophoresis
- Al:
-
Aluminum
- As:
-
Arsenic
- BGAF:
-
Beta-glucosidase aggregating factor
- Cd:
-
Cadmium
- Cr:
-
Chromium
- Cr6+ :
-
Hexavalent chromium
- Cu:
-
Copper
- Fd-GOGAT:
-
Ferredoxin-dependent glutamate synthase
- FNR:
-
Ferredoxin-NADP reductase
- GADPH:
-
Glyceraldehyde 3-phosphate dehydrogenase
- Gly I:
-
Glyoxalase I
- GS:
-
Glutamine synthetase
- GSH:
-
Glutathione
- HSP:
-
Heat shock protein
- ICDH:
-
NADP-isocitrate dehydrogenase
- K2Cr2O7 :
-
Potassium dichromate
- MALDI-TOF/TOF–MS:
-
MALDI time-of-flight/time-of-flight tandem mass spectrometer
- Mn:
-
Manganese
- NED:
-
NAD-dependent epimerase/dehydratase
- Ni:
-
Nickel
- OEC:
-
Oxygen-evolving complex
- OsVDAC:
-
Voltage-dependent anion-selective channel protein
- Pb:
-
Lead
- PC:
-
Principal component
- PCA:
-
Principal component analysis
- PGLP:
-
2-Phosphoglycolate phosphatase
- pI :
-
Isoelectric point
- RGP:
-
Reversibly glycosylated polypeptide
- ROS:
-
Reactive oxygen species
- RuBisCO:
-
Ribulose-1,5-bisphosphate carboxylase/oxygenase
- SAMS:
-
S-adenosyl-l-methionine synthetase
References
Ahsan N, Lee DG, Lee SH, Kang KY, Lee JJ, Kim PJ, Yoon HS, Kim JS, Lee BH (2007) Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere 67:1182–1193
Ahsan N, Lee DG, Alam I, Kim PJ, Lee JJ, Ahn YO, Kwak SS, Lee IJ, Bahk JD, Kang KY, Renaut J, Komatsu S, Lee BH (2008) Comparative proteomic study of arsenic-induced differentially-expressed proteins in rice roots reveals glutathione plays a central role during As stress. Proteomics 8:3561–3576
Ahsan N, Renaut J, Komatsu S (2009) Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 9:2602–2621
Ali S, Farooq MA, Jahangir MM, Abbas F, Bharwana SA, Zhang GP (2013) Effect of chromium and nitrogen form on photosynthesis and anti-oxidative system in barley. Biol Plant 57:758–763
Bah AM, Sun H, Chen F, Zhou J, Dai H, Zhang G, Wu F (2010) Comparative proteomic analysis of Typha angustifolia leaf under chromium, cadmium and lead stress. J Hazard Mater 184:191–203
Bonet A, Poschenrieder C, Barcelo J (1991) Chromium III–iron interaction in Fe-deficient and Fe-sufficient bean plants: I. growth and nutrient content. J Plant Nutr 14:403–414
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
Chen X, Kim J (2009) Callose synthesis in higher plants. Plant Signal Behav 4:489–492
Choudhury S, Panda SK (2005) Toxic effect, oxidative stress and ultrastructural changes in moss Taxithelium nepalense (Schwaegr.) Broth. under lead and chromium toxicity. Water Air Soil Pollut 167:73–90
Devos KM, Gale MD (2000) Genome relationships: the grass model in current research. Plant Cell 12:637–646
Diwan H, Khan I, Ahmad A, Iqbal M (2010) Induction of phytochelatins and antioxidant defence system in Brassica juncea and Vigna radiata in response to chromium treatment. Plant Growth Regul 61:97–107
Galvez L, Gonzalez EM, Arrese-Igor C (2005) Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J Exp Bot 56:2551–2561
Girardini JE, Khayath N, Amirante A, Dissous C, Serra E (2005) Schistosoma mansoni: Ferredoxin-NADP(H) oxidoreductase and the metabolism of reactive oxygen species. Exp Parasit 110:157–161
Goupila P, Souguira D, Ferjani E, Faure O, Hitmi A, Ledoigt G (2009) Expression of stress-related genes in tomato plants exposed to arsenic and chromium in nutrient solution. J Plant Physiol 166:1446–1452
Hajduch M, Rakwal R, Agrawal GK, Yonekura M, Pretova A (2001) High-resolution two-dimensional electrophoresis separation of proteins from metal-stressed rice (Oryza sativa L.) leaves: drastic reductions/fragmentation of ribulose-1,5-bisphosphate carboxylase/oxygenase and induction of stress-related proteins. Electrophoresis 22:2824–2831
Hawley LE, Deeb AR, Kavanaugh CM, Jacobs RGJ (2004) Treatment technologies for chromium(VI). In: Guertin J, Jacobs JA, Avakian CP (eds) Chromium (VI) handbook. CRC Press, Boca Raton, pp 275–310
Hiller S, Abramson J, Mannella C, Wagner G, Zeth K (2010) The 3D structures of VDAC represent a native conformation. Trend Biochem Sci 35:514–521
Hossain Z, Komatsu S (2013) Contribution of proteomic studies towards understanding plant heavy metal stress response. Front Plant Sci 25:310
Hossain Z, Hajika M, Komatsu S (2012) Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acid 43:2393–2416
Jamai A, Salome PA, Schilling SH, Weber AP, McClung CR (2009) Arabidopsis photorespiratory serine hydroxymethyltransferase activity requires the mitochondrial accumulation of ferredoxin-dependent glutamate synthase. Plant Cell 21:595–606
Kim DW, Rakwal R, Agrawal GK, Jung YH, Shibato J, Jwa NS, Iwahashi Y, Iwahashi H, Kim DH, IeS Shim, Usui K (2005) A hydroponic rice seedling culture model system for investigating proteome of salt stress in rice leaf. Electrophoresis 26:4521–4539
Kotas J, Stasicka Z (2000) Chromium occurrence in the environment and methods of its speciation. Environ Pollut 107:263–283
Labra M, Gianazza E, Waitt R, Eberini I, Sozzi A, Regondi S, Grassi F, Agradi E (2006) Zea mays L. protein changes in response to potassium dichromate treatments. Chemosphere 62:1234–1244
Lee JH, Chae HS, Hwang B, Hahn KW, Kang BG, Kim WT (1997) Structure and expression of two cDNAs encoding S-adenosyl-l-methionine synthetase of rice (Oryza sativa L.). Biochim Biophys Acta 1354:13–18
Lee DG, Ahsan N, Lee SH, Lee JJ, Bahk JD, Kang KY, Lee BH (2009) Chilling stress-induced proteomic changes in rice roots. J Plant Physiol 166:1–11
Lehotai N, Peto A, Bajkan S, Erdei L, Tari I, Kolbert Z (2011) In vivo and in situ visualization of early physiological events induced by heavy metals in pea root meristem. Acta Physiol Plant 33:2199–2207
Leterrier M, Del Rio LA, Corpas FJ (2007) Cytosolic NADP-isocitrate dehydrogenase of pea plants: genomic clone characterization and functional analysis under abiotic stress conditions. Free Radic Res 41:191–199
Li W, Tang X, Xing J, Sheng X, Zhan W (2014) Proteomic analysis of differentially expressed proteins in Fenneropenaeus chinensis hemocytes upon white spot syndrome virus infection. PLoS ONE 9(2):e89962
Lin RX, Zhao HB, Li CR, Sun YN, Qian XH, Wang SQ (2009) Proteomic analysis of ionizing radiation-induced proteins at the subcellular level. J Proteome Res 8:390–399
Marino D, Gonzalez EM, Frendo P, Puppo A, Arrese-Igor C (2007) NADPH recycling systems in oxidative stressed pea nodules: a key role for the NADP+-dependent isocitrate dehydrogenase. Planta 225:413–421
Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972
Nwugo CC, Huerta AJ (2011) The effect of silicon on the leaf proteome of rice (Oryza sativa L.) plants under cadmium-stress. J Proteome Res 10:518–528
Nyitrai P, Bóka K, Gáspár L, Sárvári E, Lenti K, Keresztes A (2003) Characterization of the stimulating effect of low-dose stressors in maize and bean seedlings. J Plant Physiol 160:1175–1183
Panda SK (2007) Chromium-mediated oxidative stress and ultrastructural changes in root cells of developing rice seedlings. J Plant Physiol 164:1419–1428
Perfus-Barbeoch L, Jones AM, Assmann SM (2004) Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. Curr Opin Plant Biol 7:719–731
Rana NK, Mohanpuria P, Yadav SK (2008) Expression of tea cytosolic glutamine synthetase is tissue specific and induced by cadmium and salt stress. Biol Plant 52:361–364
Rout GR, Samantaray S, Das P (2000) Effects of chromium and nickel on germination and growth in tolerant and non-tolerant populations of Echinochloa colona (L.) Link. Chemosphere 40:855–859
Sagi G, Katz A, Guenoune-Gelbart D, Epel BL (2005) Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the golgi apparatus. Plant Cell 17:1788–1800
Santos C, Pereira A, Pereira S, Teixeira J (2004) Regulation of glutamine synthetase expression in sunflower cells exposed to salt and osmotic stress. Sci Hortic 103:101–111
Sasaki T, Burr B (2000) International rice genome sequencing project: the effort to completely sequence the rice genome. Curr Opin Plant Biol 3:138–141
Saxena IM, Brown RM Jr (1999) Are the reversibly glycosylated polypeptides implicated in plant cell wall biosynthesis non-processive beta-glycosyltransferases? Trend Plant Sci 4:6–7
Schwarte S, Bauwe H (2007) Identification of the photorespiratory 2-phosphoglycolate phosphatase, PGLP1, in Arabidopsis. Plant Physiol 144:1580–1586
Seifert GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Curr Opin Plant Biol 7:277–284
Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Inter 31:739–753
Sharmin SA, Alam I, Kim K-H, Kim Y-G, Kim PJ, Bahk JD, Lee B-H (2012) Chromium-induced physiological and proteomic alterations in roots of Miscanthus sinensis. Plant Sci 187:113–126
Singh HP, Batish DR, Kaur G, Arora K, Kohli K (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167
Ueki S, Citovsky V (2002) The systemic movement of a tobamovirus is inhibited by a cadmium-ion-induced glycine-rich protein. Nat Cell Biol 4:478–486
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372
Xia J, Psychogios N, Young N, Wishart DS (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res 37:W652–W660
Xu J, Wang WY, Yin HX, Liu XJ, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330
Zavaliev R, Sagi G, Gera A, Epel BL (2010) The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J Exp Bot 61:131–142
Zeng FR, Mao Y, Cheng WD, Wu FB, Zhang GP (2008) Genotypic and environmental variation in chromium, cadmium and lead concentrations in rice. Environ Pollut 153:309–314
Zeng FR, Qiu BY, Ali S, Zhang GP (2010) Genotypic differences in nutrient uptake and accumulation in rice under chromium stress. J Plant Nutr 33:518–528
Zeng FR, Zhou WH, Qiu BY, Ali S, Wu FB, Zhang GP (2011) Subcellular distribution and chemical forms of chromium in rice plants suffering from different levels of chromium toxicity. J Plant Nutr Soil Sci 174:249–256
Zeng FR, Qiu BY, Wu XJ, Niu SZ, Wu FB, Zhang GP (2012) Glutathione-mediated alleviation of chromium toxicity in rice plants. Biol Trace Element Res 148:255–263
Zhou S, Sauve R, Thannhauser TW (2009) Proteome changes induced by aluminum stress in tomato roots. J Exp Bot 60:1849–1857
Acknowledgments
This work was supported by National Natural Science Foundation of China (31101107) and China Postdoctoral Science Foundation (20110491820). We are immensely grateful to Beijing Proteome Research Center for their expert technical assistance in 2-DE and mass spectrometry analysis.
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Supplementary Fig. S1: Two-dimensional electrophoresis (2-DE) gel maps of total leaf proteome of rice seedlings (PPTX 604 kb)
425_2014_2077_MOESM2_ESM.pptx
Supplementary Fig. S2: Two-dimensional electrophoresis (2-DE) gel maps of total root proteome of rice seedlings (PPTX 697 kb)
425_2014_2077_MOESM3_ESM.docx
Supplementary Table S1: Identification of Cr stress-induced differentially expressed RuBisCO large subunits in rice leaves by MALDI-TOF/TOF MS analysis (DOCX 120 kb)
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Zeng, F., Wu, X., Qiu, B. et al. Physiological and proteomic alterations in rice (Oryza sativa L.) seedlings under hexavalent chromium stress. Planta 240, 291–308 (2014). https://doi.org/10.1007/s00425-014-2077-3
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DOI: https://doi.org/10.1007/s00425-014-2077-3