Investigating the Contribution of the Phosphate Transport Pathway to Arsenic Accumulation in Rice
Tóm tắt
Arsenic (As) accumulation in rice (Oryza sativa) may pose a significant health risk to consumers. Plants take up different As species using various pathways. Here, we investigated the contribution of the phosphate (Pi) transport pathway to As accumulation in rice grown hydroponically or under flooded soil conditions. In hydroponic experiments, a rice mutant defective in OsPHF1 (for phosphate transporter traffic facilitator1) lost much of the ability to take up Pi and arsenate and to transport them from roots to shoots, whereas transgenic rice overexpressing either the Pi transporter OsPht1;8 (OsPT8) or the transcription factor OsPHR2 (for phosphate starvation response2) had enhanced abilities of Pi and arsenate uptake and translocation. OsPT8 was found to have a high affinity for both Pi and arsenate, and its overexpression increased the maximum influx by 3- to 5-fold. In arsenate-treated plants, both arsenate and arsenite were detected in the xylem sap, with the proportion of the latter increasing with the exposure time. Under the flooded soil conditions, the phf1 mutant took up less Pi whereas the overexpression lines took up more Pi. But there were no similar effects on As accumulation and distribution. Rice grain contained predominantly dimethylarsinic acid and arsenite, with arsenate being a minor species. These results suggest that the Pi transport pathway contributed little to As uptake and transport to grain in rice plants grown in flooded soil. Transgenic approaches to enhance Pi acquisition from paddy soil through the overexpression of Pi transporters may not increase As accumulation in rice grain.
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Tài liệu tham khảo
Abedin, 2002, Arsenic accumulation and metabolism in rice (Oryza sativa L.), Environ Sci Technol, 36, 962, 10.1021/es0101678
Abedin, 2002, Uptake kinetics of arsenic species in rice plants, Plant Physiol, 128, 1120, 10.1104/pp.010733
Ai, 2009, Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation, Plant J, 57, 798, 10.1111/j.1365-313X.2008.03726.x
Barber, 1984, Soil Nutrient Bioavailability: A Mechanistic Approach
Bienert, 2008, A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes, BMC Biol, 6, 26, 10.1186/1741-7007-6-26
Carey, 2010, Grain unloading of arsenic species in rice, Plant Physiol, 152, 309, 10.1104/pp.109.146126
Chen, 2005, Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots, New Phytol, 165, 91, 10.1111/j.1469-8137.2004.01241.x
Chiou, 2011, Signaling network in sensing phosphate availability in plants, Annu Rev Plant Biol, 62, 185, 10.1146/annurev-arplant-042110-103849
Dittmar, 2010, Arsenic in soil and irrigation water affects arsenic uptake by rice: complementary insights from field and pot studies, Environ Sci Technol, 44, 8842, 10.1021/es101962d
European Food Safety Authority, 2009, Scientific opinion on arsenic in food, EFSA Journal, 7, 1
González, 2005, PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis, Plant Cell, 17, 3500, 10.1105/tpc.105.036640
Hiei, 1997, Transformation of rice mediated by Agrobacterium tumefaciens, Plant Mol Biol, 35, 205, 10.1023/A:1005847615493
Huguenin-Elie, 2009, The effects of water regime on phosphorus responses of rainfed lowland rice cultivars, Ann Bot (Lond), 103, 211, 10.1093/aob/mcn199
Isayenkov, 2008, The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake, FEBS Lett, 582, 1625, 10.1016/j.febslet.2008.04.022
Jia, 2011, The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice, Plant Physiol, 156, 1164, 10.1104/pp.111.175240
Kile, 2007, Dietary arsenic exposure in Bangladesh, Environ Health Perspect, 115, 889, 10.1289/ehp.9462
Lee, 1982, Selectivity and kinetics of ion uptake by barley plants following nutrient deficiency, Ann Bot (Lond), 50, 429, 10.1093/oxfordjournals.aob.a086383
Li, 2009, The rice aquaporin Lsi1 mediates uptake of methylated arsenic species, Plant Physiol, 150, 2071, 10.1104/pp.109.140350
Li, 2009, Mitigation of arsenic accumulation in rice with water management and silicon fertilization, Environ Sci Technol, 43, 3778, 10.1021/es803643v
Liu, 2010, OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice, Plant J, 62, 508, 10.1111/j.1365-313X.2010.04170.x
Liu, 2010, Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis, Plant Physiol, 152, 2211, 10.1104/pp.109.150862
Liu, 2006, Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza sativa L.), Environ Sci Technol, 40, 5730, 10.1021/es060800v
Ma, 2008, Transporters of arsenite in rice and their role in arsenic accumulation in rice grain, Proc Natl Acad Sci USA, 105, 9931, 10.1073/pnas.0802361105
Meharg, 1994, Phosphorus nutrition of arsenate tolerant and nontolerant phenotypes of velvetgrass, J Environ Qual, 23, 234, 10.2134/jeq1994.00472425002300020003x
Meharg, 2003, Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption, Environ Sci Technol, 37, 229, 10.1021/es0259842
Meharg, 2009, Geographical variation in total and inorganic arsenic content of polished (white) rice, Environ Sci Technol, 43, 1612, 10.1021/es802612a
Mitsukawa, 1997, Overexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions, Proc Natl Acad Sci USA, 94, 7098, 10.1073/pnas.94.13.7098
Mondal, 2008, Rice is a major exposure route for arsenic in Chakdaha block, Nadia district, West Bengal, India: a probabilistic risk assessment, Appl Geochem, 23, 2987, 10.1016/j.apgeochem.2008.06.025
Moore, 2011, NanoSIMS analysis reveals contrasting patterns of arsenic and silicon localization in rice roots, Plant Physiol, 156, 913, 10.1104/pp.111.173088
Norton, 2010, Arsenic shoot-grain relationships in field grown rice cultivars, Environ Sci Technol, 44, 1471, 10.1021/es902992d
Panaullah, 2009, Arsenic toxicity to rice (Oryza sativa L.) in Bangladesh, Plant Soil, 317, 31, 10.1007/s11104-008-9786-y
Paszkowski, 2002, Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis, Proc Natl Acad Sci USA, 99, 13324, 10.1073/pnas.202474599
Raab, 2005, Uptake, translocation and transformation of arsenate and arsenite in sunflower (Helianthus annuus): formation of arsenic-phytochelatin complexes during exposure to high arsenic concentrations, New Phytol, 168, 551, 10.1111/j.1469-8137.2005.01519.x
Raab, 2007, Uptake and translocation of inorganic and methylated arsenic species by plants, Environ Chem, 4, 197, 10.1071/EN06079
Rae, 2004, Over-expression of a high-affinity phosphate transporter in transgenic barley plants does not enhance phosphate uptake rates, Funct Plant Biol, 31, 141, 10.1071/FP03159
Raghothama, 1999, Phosphate acquisition, Annu Rev Plant Physiol Plant Mol Biol, 50, 665, 10.1146/annurev.arplant.50.1.665
Rubio, 2001, A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae, Genes Dev, 15, 2122, 10.1101/gad.204401
Schmöger, 2000, Detoxification of arsenic by phytochelatins in plants, Plant Physiol, 122, 793, 10.1104/pp.122.3.793
Seyfferth, 2010, Arsenic localization, speciation, and co-occurrence with iron on rice (Oryza sativa L.) roots having variable Fe coatings, Environ Sci Technol, 44, 8108, 10.1021/es101139z
Shin, 2004, Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments, Plant J, 39, 629, 10.1111/j.1365-313X.2004.02161.x
Silberbush, 1983, Sensitivity of simulated phosphorus uptake to parameters used by a mechanistic mathematical model, Plant Soil, 74, 93, 10.1007/BF02178744
Song, 2010, Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters, Proc Natl Acad Sci USA, 107, 21187, 10.1073/pnas.1013964107
Stroud, 2011, The dynamics of arsenic in four paddy fields in the Bengal delta, Environ Pollut, 159, 947, 10.1016/j.envpol.2010.12.016
Takahashi, 2004, Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods, Environ Sci Technol, 38, 1038, 10.1021/es034383n
Tsuji, 2007, Use of background inorganic arsenic exposures to provide perspective on risk assessment results, Regul Toxicol Pharmacol, 48, 59, 10.1016/j.yrtph.2007.01.004
Ullrich-Eberius, 1989, Evaluation of arsenate- and vanadate-associated changes of electrical membrane potential and phosphate transport in Lemna gibba-G1, J Exp Bot, 40, 119, 10.1093/jxb/40.1.119
Williams, 2005, Variation in arsenic speciation and concentration in paddy rice related to dietary exposure, Environ Sci Technol, 39, 5531, 10.1021/es0502324
Williams, 2007, Market basket survey shows elevated levels of As in South Central U.S. processed rice compared to California: consequences for human dietary exposure, Environ Sci Technol, 41, 2178, 10.1021/es061489k
Williams, 2007, Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley, Environ Sci Technol, 41, 6854, 10.1021/es070627i
Xu, 2008, Growing rice aerobically markedly decreases arsenic accumulation, Environ Sci Technol, 42, 5574, 10.1021/es800324u
Ye, 2010, Arsenic speciation in phloem and xylem exudates of castor bean, Plant Physiol, 154, 1505, 10.1104/pp.110.163261
Zhao, 2010, The role of the rice aquaporin Lsi1 in arsenite efflux from roots, New Phytol, 186, 392, 10.1111/j.1469-8137.2010.03192.x
Zhao, 2009, Arsenic uptake and metabolism in plants, New Phytol, 181, 777, 10.1111/j.1469-8137.2008.02716.x
Zhao, 2010, Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies, Annu Rev Plant Biol, 61, 535, 10.1146/annurev-arplant-042809-112152
Zhou, 2008, OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants, Plant Physiol, 146, 1673, 10.1104/pp.107.111443