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Proteomic changes of Citrus roots in response to long-term manganese toxicity

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Fifty-three and thirty-nine differentially expressed protein spots were isolated from Mn-toxic Citrus sinensis and Citrus grandis roots, respectively. Mn-toxicity-induced changes in protein profiles greatly differed between the two species.

Abstract

Limited information is available on the manganese (Mn)-toxicity-responsive proteins in plant roots. ‘Sour pummelo’ (Citrus grandis) and ‘Xuegan’ (Citrus sinensis) seedlings were irrigated for 17 weeks with 2 (control) or 600 μM (Mn-toxic) MnSO4. C. sinensis displayed more tolerance to Mn-toxicity than C. grandis, which may be related to more Mn accumulation in roots and less Mn distribution in shoots. Using two-dimensional electrophoresis (2-DE), we isolated 11 up-regulated and 42 down-regulated protein spots from Mn-toxic C. sinensis roots, and 25 up-regulated and 14 down-regulated protein spots from Mn-toxic C. grandis roots. This indicated more metabolic flexibility in C. sinensis roots, thus contributing to the Mn-tolerance of C. sinensis. According to the biological functional properties, these differentially expressed proteins in the two species were classified into the following categories: protein metabolism, nucleic acid metabolism, carbohydrate and energy metabolism, stress responses, cell wall and cytoskeleton, cell transport, signal transduction and fatty acid metabolism. Under Mn-toxicity, proteins involved in nucleic acid metabolism, glycolysis and cell transport were up-regulated in nontolerant C. grandis roots, and down-regulated in tolerant C. sinensis roots. The notable down-regulation of proteins in Mn-toxic C. sinensis roots with less accumulation of carbohydrates may provide an advantage to the net carbon balance by lowering related metabolic processes, and enhancing the Mn-tolerance of C. sinensis. To conclude, there are many important differences in Mn-toxicity-induced changes in protein profiles and metabolic responses between the two species.

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References

  • Bidwell SD, Woodrow IE, Batianoff GN, Sommer-Knudsen J (2002) Hyperaccumulation of manganese in the rainforest tree Austromyrtus bidwillii (Myrtaceae) from Queensland, Australia. Funct Plant Biol 29:899–905

    Article  CAS  Google Scholar 

  • Boerjan W, Bauw G, Van Montagu M, Inzé D (1994) Distinct phenotypes generated by overexpression and suppression of S-adenosyl-l-methionine synthetase reveal developmental patterns of gene silencing in tobacco. Plant Cell 6:1401–1414

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Boojar MMA, Goodarzi F (2008) Comparative evaluation of oxidative stress status and manganese availability in plants growing on manganese mine. Ecotoxicol Environ Safe 71:692–699

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram and quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cai G (2010) Assembly and disassembly of plant microtubules: tubulin modifications and binding to MAPs. J Exp Bot 61:623–626

    Article  PubMed  CAS  Google Scholar 

  • Cheng Y, Long M (2007) A cytosolic NADP-malic enzyme gene from rice (Oryza sativa L.) confers salt tolerance in transgenic Arabidopsis. Biotechnol Let 29:1129–1134

    Article  CAS  Google Scholar 

  • DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5:663–667

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dietz KJ, Tavakoli N, Kluge C, Mimura T, Sharma SS, Harris GC, Chardonnens AN, Golldack D (2001) Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot 52:1969–1980

    Article  PubMed  CAS  Google Scholar 

  • Dučić TD, Leinemann L, Finkeldey R, Polle A (2006) Uptake and translocation of manganese in seedlings of two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca). New Phytol 170:11–20

    Article  PubMed  Google Scholar 

  • Durst F (1976) Correlation of phenylalanine ammonia-lyase and cinnamic acid hydroxylase activity changes in Jerusalem artichoke tuber tissues. Planta 132:221–227

    Article  PubMed  CAS  Google Scholar 

  • Eason JR, Ryan DJ, Pinkney TT, O’Donoghue EM (2002) Programmed cell death during flower senescence: isolation and characterization of cysteine proteinases from Sandersonia aurantiaca. Funct Plant Biol 29:1055–1064

    Article  CAS  Google Scholar 

  • Fecht-Christoffers M, Braun HP, Christelle Lemaitre-Guillier C, VanDorsselaer A, Walter J, Horst WJ (2003) Effect of manganese toxicity on the proteome of the leaf apoplast in cowpea. Plant Physiol 133:1935–1946

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fecht-Christoffers MM, Führs H, Braun H-P, Horst WJ (2006) The role of hydrogen peroxide-producing and hydrogen peroxide consuming peroxidases in the leaf apoplast of cowpea in manganese tolerance. Plant Physiol 140:1451–1463

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fernando DR, Mizuno T, Woodrow IE, Baker AJ, Collins RN (2010) Characterization of foliar manganese (Mn) in Mn (hyper)accumulators using X-ray absorption spectroscopy. New Phytol 188:1014–1027

    Article  PubMed  CAS  Google Scholar 

  • Ferrell K, Wilkinson CRM, Dubiel W, Gordon C (2000) Regulatory subunit interactions of the 26S proteasome, a complex problem. Trends Biochem Sci 25:83–88

    Article  PubMed  CAS  Google Scholar 

  • Foy CD (1984) Physiological effects of hydrogen, aluminum, and manganese toxicities in acid soils. In: Adams J (ed) Soil acidity and liming, 2nd edn. American Society of Agronomy, Madison, pp 57–97

    Google Scholar 

  • Führs H, Hartwig M, Molina LE, Heintz D, Van Dorsselaer A, Braun HP, Horst WJ (2008) Early manganese-toxicity response in Vigna unguiculata L.—a proteomic and transcriptomic study. Proteomics 8:149–159

    Article  PubMed  Google Scholar 

  • Führs H, Götze S, Specht A, Erban A, Gallien S, Heintz D, Van Dorsselaer A, Kopka J, Braun HP, Horst WJ (2009) Characterization of leaf apoplastic peroxidases and metabolites in Vigna unguiculata in response to toxic manganese supply and silicon. J Exp Bot 60:1663–1678

    Article  PubMed  PubMed Central  Google Scholar 

  • Führs H, Behrens C, Gallien S, Heintz H, Van Dorsselaer A, Braun HP, Horst WJ (2010) Physiological and proteomic characterization of manganese sensitivity and tolerance in rice (Oryza sativa) in comparison with barley (Hordeum vulgare). Ann Bot 105:1129–1140

    Article  PubMed  PubMed Central  Google Scholar 

  • Führs H, Specht A, Erban A, Kopka J, Horst WJ (2012) Functional associations between the metabolome and manganese tolerance in Vigna unguiculata. J Exp Bot 63:329–340

    Article  PubMed  PubMed Central  Google Scholar 

  • Gangwar S, Singh VP, Prasad SM, Maurya JN (2010) Modulation of manganese toxicity in Pisum sativum L. seedlings by kinetin. Sci Hort 126:467–474

    Article  CAS  Google Scholar 

  • Gherardi MJ, Rengel Z (2003) Genotypes of lucerne (Medicago sativa L.) show differential tolerance to manganese deficiency and toxicity when grown in bauxite residue sand. Plant Soil 249:287–296

    Article  CAS  Google Scholar 

  • Gichner T, Patková Z, Száková J, Demnerová K (2006) Toxicity and DNA damage in tobacco and potato plants growing on soil polluted with heavy metals. Ecotoxicol Environ Safe 65:420–426

    Article  CAS  Google Scholar 

  • Gillet S, Decottignies P, Chardonnet S, Le Maréchal P (2006) Cadmium response and redoxin targets in Chlamydomonas reinhardtii: a proteomic approach. Photosynth Res 89:201–211

    Article  PubMed  CAS  Google Scholar 

  • González A, Steffen KL, Lynch JP (1998) Light and excess manganese implications for oxidative stress in common bean. Plant Physiol 118:493–504

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KW, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010

    Article  PubMed  CAS  Google Scholar 

  • Han S, Tang N, Jiang HX, Yang LT, Li Y, Chen LS (2009) CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress. Plant Sci 176:143–153

    Article  CAS  Google Scholar 

  • Harrak H, Azelmat S, Baker EN, Tabaeizadeh Z (2001) Isolation and characterization of a gene encoding a drought-induced cysteine protease in tomato (Lycopersicon esculentum). Genome 44:368–374

    Article  PubMed  CAS  Google Scholar 

  • Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473–503

    Article  PubMed  CAS  Google Scholar 

  • Hossain Z, Komatsu S (2013) Contribution of proteomic studies towards understanding plant heavy metal stress response. Front Plant Sci 3:310

    Article  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Janicka-Russak M, Kabała K, Burzyński M, Kłobus G (2008) Response of plasma membrane H+-ATPase to heavy metal stress in Cucumis sativus roots. J Exp Bot 59:3721–3728

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jiang XM, Neal B, Santiago F, Lee SJ, Romana LK, Reeves PR (1991) Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2). Mol Microbiol 5:695–713

    Article  PubMed  CAS  Google Scholar 

  • Kabała K, Janicka-Russak M (2011) Differential regulation of vacuolar H+-ATPase and H+-PPase in Cucumis sativus roots by zinc and nickel. Plant Sci 180:531–539

    Article  PubMed  Google Scholar 

  • Kato-Noguchi H (2008) Low temperature acclimation mediated by ethanol production is essential for chilling tolerance in rice roots. Plant Signal Behav 3:202–203

    Article  PubMed  PubMed Central  Google Scholar 

  • Kinoshita T, Yamada K, Hiraiwa N, Kondo M, Nishimura M, Hara-Nishimura I (1999) Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. Plant J 19:43–53

    Article  PubMed  CAS  Google Scholar 

  • Kitao M, Lei TT, Koike T (1997) Effects of manganese toxicity on photosynthesis of white birch (Betula platyphylla var. japonica) seedlings. Physiol Plant 101:249–256

    Article  CAS  Google Scholar 

  • Kochevenko A, Fernie AR (2011) The genetic architecture of branched-chain amino acid accumulation in tomato fruits. J Exp Bot 62:3895–3906

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • LeClere S, Tellez R, Rampey RA, Matsuda SPT, Bartel B (2002) Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J Biol Chem 277:20446–20452

    Article  PubMed  CAS  Google Scholar 

  • Lee TJ, Luitel BP, Kang WH (2011) Growth and physiological response to manganese toxicity in Chinese cabbage (Brassica rapa L. ssp. campestris). Hort Environ Biotechnol 52:252–258

    Article  CAS  Google Scholar 

  • Li Q, Chen LS, Jiang HX, Tang N, Yang LT, Lin ZH, Yang GH (2010) Effects of manganese-excess on CO2 assimilation, ribulose-1, 5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. BMC Plant Biol 10:42

    Article  PubMed  PubMed Central  Google Scholar 

  • Lidon F (2000) Tolerance of rice to excess manganese in the early stages of vegetative growth. Characterization of manganese accumulation. J Plant Physiol 158:1341–1348

    Article  Google Scholar 

  • López-Millán AF, Ellis DR, Grusak MA (2005) Effect of zinc and manganese supply on the activities of superoxide dismutase and carbonic anhydrase in Medicago truncatula wild type and raz mutant plants. Plant Sci 168:1015–1022

    Article  Google Scholar 

  • Luan S (2003) Protein phosphatase in plants. Annu Rev Plant Biol 54:63–92

    Article  PubMed  CAS  Google Scholar 

  • Maksimović JD, Mojović M, Maksimović V, Römheld V, Nikolic M (2012) Silicon ameliorates manganese toxicity in cucumber by decreasing hydroxyl radical accumulation in the leaf apoplast. J Exp Bot 63:2411–2420

    Article  PubMed  Google Scholar 

  • Mandal C, Ghosh N, Dey N, Adak MK (2013) Physiological responses of Salvinia natans L. to aluminium stress and its interaction with putrescine. J Stress Physiol Biochem 9:163–179

    Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, San Diego

    Google Scholar 

  • McHargue JS (1922) The role of manganese in plants. J Am Chem Soc 44:1592–1598

    Article  CAS  Google Scholar 

  • Meyer T, Hölscher C, Schwöppe C, von Schaewen A (2011) Alternative targeting of Arabidopsis plastidic glucose-6-phosphate dehydrogenase G6PD1 involves cysteine-dependent interaction with G6PD4 in the cytosol. Plant J 66:745–758

    Article  PubMed  CAS  Google Scholar 

  • Michopoulos P, Cresser MS (2002) Effects of simulated acid precipitation on the cycling of manganese under stika spruce (Picea sitchensis). Biogeochemistry 61:323–325

    Article  CAS  Google Scholar 

  • Millaleo R, Reyes-Díaz M, Ivanov AG, Mora ML, Alberdi M (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr 10:476–494

    Article  Google Scholar 

  • Millaleo R, Reyes-Díaz M, Alberdi M, Ivanov AG, Krol M, Hüner NPA (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Bot 64:343–354

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mills HA, Jones JB Jr (1996) Plant analysis II. MicroMacro Publishing, Georgia

    Google Scholar 

  • Minhas D, Grover A (1999) Transcript levels of genes encoding various glycolytic and fermentation enzymes change in response to abiotic stresses. Plant Sci 146:41–51

    Article  CAS  Google Scholar 

  • Mukhopadhyay MJ, Sharma A (1991) Manganese in cell metabolism of higher plants. Bot Rev 57:117–149

    Article  Google Scholar 

  • Oka T, Nemoto T, Jigami Y (2007) Functional analysis of Arabidopsis thaliana RHM2/MUM4 a multidomain protein involved in UDP-D glucose to UDP-L-rhamnose conversion. J Biol Chem 282:5389–5403

    Article  PubMed  CAS  Google Scholar 

  • Papadakis IE, Giannakoula A, Therios IN, Bosabalidis AM, Moustakas M, Nastou A (2007) Mn-induced changes in leaf structure and chloroplast ultrastructure of Citrus volkameriana (L.) plants. J Plant Physiol 164:100–103

    Article  PubMed  CAS  Google Scholar 

  • Peters JS, Frenkel C (2004) Relationship between alcohol dehydrogenase activity and low-temperature in two maize genotypes, Silverado F1 and Adh1−Adh2− doubly null. Plant Physiol Biochem 42:841–846

    Article  PubMed  CAS  Google Scholar 

  • Radyuk SN, Sohar RS, Orr WC (2003) Thioredoxin peroxidases can foster cytoprotection or cell death in response to different stressors: over- and under-expression of thioredoxin peroxidase in Drosophila cells. Biochem J 371:743–752

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rucińska R, Waplak S, Gwóźdź EA (1999) Free radical formation and activity of antioxidant enzymes in lupin roots exposed to lead. Plant Physiol Biochem 37:187–194

    Article  Google Scholar 

  • Shi Q, Zhu Z, Xu M, Qian Q, Yu J (2006) Effect of excess manganese on the antioxidant system in Cucumis sativus L. under two light intensities. Environ Exp Bot 58:197–205

    Article  CAS  Google Scholar 

  • Ślaski JJ, Zhang G, Basu U, Stephens JL, Taylor GJ (1996) Aluminum resistance in wheat (Triticum aestivum) is associated with rapid, Al-induced changes in activities of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase in root apices. Physiol Plant 98:477–484

    Article  Google Scholar 

  • Srivastava AK, Singh S (2006) Biochemical markers and nutrient constraints diagnosis in citrus: a perspective. J Plant Nutr 29:827–855

    Article  CAS  Google Scholar 

  • Van Assche F, Cardinaels C, Clijsters H (1998) Induction of enzyme capacity in plants as a result of heavy metal toxicity: dose-response relations in Phaseolus vulgaris L., treated with zinc and cadmium. Environ Pollut 52:103–115

    Article  Google Scholar 

  • Venkatesan S, Hemalatha KV, Jayaganesh S (2007) Characterization of manganese toxicity and its influence on nutrient uptake, antioxidant enzymes and biochemical parameters in tea. Res J Phytochem 1:52–60

    Article  Google Scholar 

  • Vose PB, Randall PJ (1962) Resistance to aluminum and manganese toxicities in plants related to variety and cation exchange capacity. Nature 196:85–86

    Article  CAS  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Nakazato T, Kinya Sakanishi K, Yamada O, Tao H, Saito I (2006) Single-step microwave digestion with HNO3 alone for determination of trace elements in coal by ICP spectrometry. Talanta 68:1584–1590

    Article  PubMed  CAS  Google Scholar 

  • Xu FX, Chye ML (1999) Expression of cysteine proteinase during developmental events associated with programmed cell death in brinjal. Plant J 17:321–327

    Article  PubMed  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Let 579:6265–6271

    Article  CAS  Google Scholar 

  • Yamauchi Y, Hasegawa A, Taninaka A, Mizutani M, Sugimoto Y (2011) NADPH-dependent reductases involved in the detoxification of reactive carbonyls in plants. J Biol Chem 286:6999–7009

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yang LT, Qi YP, Lu YB, Guo P, Sang W, Feng H, Zhang HX, Chen LS (2013) iTRAQ protein profile analysis of Citrus sinensis roots in response to long-term boron-deficiency. J Proteomics 93:179–206

    Article  PubMed  CAS  Google Scholar 

  • Yao Y, Xu G, Mou D, Wang J, Ma J (2012) Subcellular Mn comparation, anatomic and biochemical changes of two grape varieties in response to excess manganese. Chemosphere 89:150–157

    Article  PubMed  CAS  Google Scholar 

  • Zeng W, Chatterjee M, Faik A (2008) UDP-xylose-stimulated glucuronyltransferase activity in wheat microsomal membranes: characterization and role in glucurono (arabino) xylan biosynthesis. Plant Physiol 147:78–91

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhou CP, Qi YP, You X, Yang LT, Guo P, Ye X, Zhou XX, Ke FJ, Chen LS (2013) Leaf cDNA-AFLP analysis of two citrus species differing in manganese tolerance in response to long-term manganese-toxicity. BMC Genom 14:621

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the earmarked fund for China Agriculture Research System. The authors wish to thank Dr. Brandon R. Smith, USDA-NRCS, 2 Madbury Road, Durham NH 03824, USA and Prof. Ming-Kuang Wang, Department of Agricultural Chemistry, National Taiwan University, Taipei 106, Taiwan, for language correction and constructive comments on this manuscript.

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You, X., Yang, LT., Lu, YB. et al. Proteomic changes of Citrus roots in response to long-term manganese toxicity. Trees 28, 1383–1399 (2014). https://doi.org/10.1007/s00468-014-1042-x

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