Abstract
The effects of phosphorus (P) status on arsenate reductase gene (OsACR2.1) expression, arsenate reductase activity, hydrogen peroxide (H2O2) content, and arsenic (As) species in rice seedlings which were exposed to arsenate after −P or +P pretreatments were investigated in a series of hydroponic experiments. OsACR2.1 expression increased significantly with decreasing internal P concentrations; more than 2-fold and 10-fold increases were found after P starvation for 30 h and 14 days, respectively. OsACR2.1 expression exhibited a significant positive correlation with internal root H2O2 accumulation, which increased upon P starvation or exposure to H2O2 without P starvation. Characterization of internal and effluxed As species showed the predominant form of As was arsenate in P-starved rice root, which contrasted with the +P pretreated plants. Additionally, more As was effluxed from P-starved rice roots than from non-starved roots. In summary, an interesting relationship was observed between P-starvation induced H2O2 and OsACR2.1 gene expression. However, the up-regulation of OsACR2.1 did not increase arsenate reduction in P-starved rice seedlings when exposed to arsenate.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128 doi:10.1104/pp.010733
Alvarez ME, Penell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784 doi:10.1016/S0092-8674(00)81405-1
Bailey-Serres J, Mittler R (2006) The roles of reactive oxygen species in plant cells. Plant Physiol 141:311 doi:10.1104/pp.104.900191
Baldwin JC, Athikkattuvalasu SK, Raghothama KG (2001) LEPS2, a phosphorus starvation-induced novel acid phosphatase from tomato. Plant Physiol 125:728–737 doi:10.1104/pp.125.2.728
Bennett M, Bellini C, Straeten DVD (2005) Integrative biology: dissecting cross-talk between plant signalling pathways. Physiol Plant 123:109 doi:10.1111/j.1399-3054.2005.00483.x
Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252 doi:10.1146/annurev.pp.24.060173.001301
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 doi:10.1016/0003-2697(76)90527-3
Chen XP, Zhu YG, Hong MN, Kappler A, Xu YX (2008) Effects of different forms of nitrogen fertilizers on arsenic uptake by rice plants. Environ Toxicol Chem 27:881–887 doi:10.1897/07-368.1
Delnomdedieu M, Basti MM, Thomas DJ (1994) Reduction and binding of arsenate and dimethylarsinate by glutathione: a magnetic resonance study. Chem Biol Interact 90:139–155 doi:10.1016/0009-2797(94)90099-X
del Pozo JC, Allona I, Rubio V, Layva A, de la Peña A, Aragoncillo C et al (1999) A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilizing/oxidative stress conditions. Plant J 19:579–589 doi:10.1046/j.1365-313X.1999.00562.x
Desikan R, Neill SJ, Hancock JT (2000) Hydrogen peroxide-induced gene expression in Arabidoposis thaliana. Free Radic Biol Med 28:773–778 doi:10.1016/S0891-5849(00)00157-X
Dhankher OP, Rosen BP, McKinney EC, Meagher RB (2006) Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase, ACR2. Proc Natl Acad Sci USA 103:5413–5418 doi:10.1073/pnas.0509770102
Duan GL, Zhu YG, Tong YP, Cai C, Kneer R (2005) Characterization of arsenate reducatse in the extract of root and fronds of Chinese brake fern, an arsenic hyperaccumuator. Plant Physiol 138:461–469 doi:10.1104/pp.104.057422
Duan GL, Zhou Y, Tong YP, Mukhopadhyay R, Rosen BP, Zhu YG (2007) A CDC25 homologue from rice functions as an arsenate reductase. New Phytol 174:311–321 doi:10.1111/j.1469-8137.2007.02009.x
Duff SM, Plaxton WC, Lefebvre DD (1991) Phosphate-starvation response in plant cells: de novo synthesis and degradation of acid phosphatases. Proc Natl Acad Sci USA 88:9538–9542 doi:10.1073/pnas.88.21.9538
Ellis DR, Gumaelius L, Indriolo E, Pickering IJ, Banks JA, Salt DE (2006) Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ Sci Technol 15:5010–5014
Fageria NK (1976) Critical level P, K, Ca and Mg contents in the tops of rice and peanut plants. Plant Soil 45:421–431 doi:10.1007/BF00011704
Geng CN, Zhu YG, Hu Y, Williams PN, Meharg AA (2006) Arsenate causes differential acute toxicity to two P-deprived genotypes of rice seedlings. Plant Soil 279:297–306 doi:10.1007/s11104-005-1813-7
Heikens (2006) Arsenic contamination of irrigation water, soil and crops in Bangladesh: risk implications for sustainable agriculture and food safety in Asia. Rap Publication 2006/20. FAO, Bangkok
Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651 doi:10.1016/j.bbrc.2006.04.140
Joo JH, Bae YS, Lee JS (2001) Role of auxin-indunced reactive oxygen species in root gravitopism. Plant Physiol 126:1055–1060 doi:10.1104/pp.126.3.1055
Landrieu I, Da Costa M, De Veylder L, Dewitte F, vandepoele K, Hassan S, Wieruszeski JM, Faure JD, Montagu MV, Inze D, Lippens G (2004) A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:13380–13385 doi:10.1073/pnas.0405248101
Mascher R, Lippmann B, Holzinger S, Bergmann H (2002) Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Sci 163:961–969 doi:10.1016/S0168-9452(02)00245-5
Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol 154:29–43 doi:10.1046/j.1469-8137.2002.00363.x
Meharg AA, Jardine L (2003) Arsenite transport into paddy rice (Oryza sativa) roots. New Phytol 157:39–44 doi:10.1046/j.1469-8137.2003.00655.x
Mulherjee SP, Choudhuri MA (1983) Determination of glycolate oxidase activity, H2O2 content and catalase activity. Physiol Plant 58:167–170
Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191
Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Mol Biol 50:665–693 doi:10.1146/annurev.arplant.50.1.665
Rosen BP (2002) Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comp Biochem Physiol A Mol Integr Physiol 133:689–693 doi:10.1016/S1095-6433(02)00201-5
Runge-Metzger A (1995) Closing the cycle: obstacles to efficient P management for improved global security. In: Tiessen H (ed) Phosphorus in the global environment. Wiley, Chichester, UK, pp 27–42
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
Schachtman DP, Shin R (2007) Nutrient Sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69 doi:10.1146/annurev.arplant.58.032806.103750
Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832 doi:10.1073/pnas.0401707101
Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357 doi:10.1093/pcp/pci145
Smith AH, Hopenhaynrich C, Bates MN, Goeden HM, Hertzpicciotto I, Duggan HM et al (1992) Cancer risks from arsenic in drinking-water. Environ Health Perspect 97:259–267 doi:10.2307/3431362
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447 doi:10.1046/j.1469-8137.2003.00695.x
von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15 doi:10.1007/BF00009558
Wang LH, Meng XY, Guo B, Duan GL (2007) Reduction of arsenic oxidative toxicity by phosphate is not related to arsenic reductase activity in wheat plants. J Plant Nutr 30:2105–2117 doi:10.1080/01904160701700582
Williams PN, Villada A, Deacon C, Raab A, Figuerola J, Green AJ et al (2007) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat & barley. Environ Sci Technol 41:6854–6859 doi:10.1021/es070627i
Xu YX, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176:590–599 doi:10.1111/j.1469-8137.2007.02195.x
Zhou Y, Bhattacharjee H, Mukhopadhyay R (2006) Bifunctional role of the leishmanial antimonate reductase LmACR2 as a protein tyrosine phosphatase. Mol Biochem Parasitol 148:161–168 doi:10.1016/j.molbiopara.2006.03.009
Zhu YG, Williams PN, Meharg AA (2008a) Exposure to inorganic arsenic from rice: aglobal health issue? Environ Pollut 154:169–171
Zhu YG, Sun G X, Lei M, Teng M, Liu YX, Chen NC, Wang LH, CareyAM, Deacon C, Raab A, Meharg AA, Williams PN (2008b). High percentage inorganic arsenic content of mining impacted and non-impacted Chinese rice. Environ Sci Technol. doi:10.1021/es8001103
Acknowledgments
This project was financially supported by the Natural Science Foundation of China (20720102042 and 20777083) and Ministry of Science and Technology of China (2002CB410808). In addition, we recognize the support in the form of a Chinese Academy of Science’s “Research Fellowship for International Young Researchers” and funds from the Royal Society of Edinburgh’s International Exchange programme to P.N.W. We appreciate the helpful discussion with Dr H. Christophersen.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Fangjie J. Zhao.
Rights and permissions
About this article
Cite this article
Wang, LH., Duan, GL., Williams, P.N. et al. Influences of phosphorus starvation on OsACR2.1 expression and arsenic metabolism in rice seedlings. Plant Soil 313, 129–139 (2008). https://doi.org/10.1007/s11104-008-9685-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-008-9685-2