When does temperature matter? Response of rice arsenic to heat exposure during different developmental stages
Tóm tắt
Arsenic is a frequent contaminant of rice. Recent studies show that elevated temperatures, like those from climate change, can further increase arsenic concentrations in rice. It is still unclear if the timing of heat exposure relative to plant development influences the magnitude and allocation of arsenic accumulation in rice plants. We grew potted rice plants from seedlings until maturity in growth chambers with different temperature regimes: baseline (26 °C/22 °C, day/night), continuously elevated (30 °C/27 °C), baseline with a 20-day heat spike during the vegetative stage, and baseline with a 20-day heat spike during the ripening stage. Heat spikes mimicked the elevated temperature. Concentrations of arsenic in both porewater and plant tissues were uniformly higher in the continuously elevated treatment relative to the baseline treatment. A heat spike during the ripening stage caused a marked increase in arsenic mobilization into porewater. A heat spike in the vegetative stage caused a short-term increase in arsenic concentrations in plant tissue but this relative increase did not persist to maturity. Plants that experienced a heat spike in the ripening stage had an increase in arsenic concentrations within various tissue types at maturity. Differential responses to the two heat spikes may be due to less soil microbial and plant biomass during the vegetative stage, as well as reduced root biomass caused by heat stress during the vegetative stage. Our results demonstrate that both continuous and short-term increases in temperature later in plant development can heighten dietary arsenic exposure to rice consumers.
Tài liệu tham khảo
Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128. https://doi.org/10.1104/pp.010733
Ahmann D, Krumholz LR, Hemond HF, Lovley DR, Morel FMM (1997) Microbial mobilization of arsenic from sediments of the Aberjona watershed. Environ Sci Technol 31:2923–2930. https://doi.org/10.1021/es970124k
Arao T, Kawasaki A, Baba K, Mori S, Matsumoto S (2009) Effects of water management on cadmium and arsenic accumulation and dimethylarsinic acid concentrations in Japanese rice. Environ Sci Technol 43:9361–9367. https://doi.org/10.1021/es9022738
Arao T, Makino T, Kawasaki A, Akahane I, Kiho N (2018) Effect of air temperature after heading of rice on the arsenic concentration of grain. Soil Sci Plant Nutr 64:433–437. https://doi.org/10.1080/00380768.2018.1438811
Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148. https://doi.org/10.1055/s-2001-12905
Azizur Rahman M, Hasegawa H, Mahfuzur Rahman M, Nazrul Islam M, Majid Miah MA, Tasmen A (2007) Effect of arsenic on photosynthesis, growth and yield of five widely cultivated rice (Oryza sativa L.) varieties in Bangladesh. Chemosphere 67:1072–1079. https://doi.org/10.1016/j.chemosphere.2006.11.061
Beare MH, Coleman DC, Crossley DA, Hendrix PF, Odum EP (1995) A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. Plant Soil 170:5–22. https://doi.org/10.1007/BF02183051
Carrijo DR, Li C, Parikh SJ, Linquist BA (2019) Irrigation management for arsenic mitigation in rice grain: Timing and severity of a single soil drying. Sci Total Environ 649:300–307. https://doi.org/10.1016/j.scitotenv.2018.08.216
Chang AC, Page AL, Krage NJ (2004) Role of Fertilizer and Micronutrient Applications on Arsenic, Cadmium, and Lead Accumulation in California Cropland Soils. California Department of Agriculture, Riverside, California
Chen C, Yang B, Shen Y, Dai J, Tang Z, Wang P, Zhao F-J (2021) Sulfate addition and rising temperature promote arsenic methylation and the formation of methylated thioarsenates in paddy soils. Soil Biol Biochem 154:108129. https://doi.org/10.1016/j.soilbio.2021.108129
Chi Y, Li F, Tam NF-Y, Liu C, Ouyang Y, Qi X, Li WC, Ye Z (2018) Variations in grain cadmium and arsenic concentrations and screening for stable low-accumulating rice cultivars from multi-environment trials. Sci Total Environ 643:1314–1324. https://doi.org/10.1016/j.scitotenv.2018.06.288
Cline G, Neigher A, Bellinder A (2010) Climate of Sacramento, California. National Weather Service, Sacramento California
Codex Alimentarius Commission (2014) Report of the either session of the codex committee on contaminants in foods. Joint FAO/WHO Food Standards Programme, Geneva, Switzerland
Consumer Reports (2014) How much arsenic is in your rice? Available at https://www.consumerreports.org/cro/magazine/2015/01/how-much-arsenic-is-in-your-rice/index.htm
Dhar P, Kobayashi K, Ujiie K, Adachi F, Kasuga J, Akahane I, Arao T, Matsumoto S (2020) The Increase in the arsenic concentration in brown rice due to high temperature during the ripening period and its reduction by silicate material treatment. Agriculture 10. https://doi.org/10.3390/agriculture10070289.
Dhar P, Kasuga J, Koyama Y, Fujisaki K, Kadowaki M, Kobayasi K, Matsumoto S (2022) Factors causing the increase in arsenic concentration in brown rice due to high temperatures during the ripening period and its reduction by applying converted furnace slag. J Plant Nutr: 1–24. https://doi.org/10.1080/01904167.2022.2160746
Fageria NK (2014) Mineral nutrition of rice. CRC Press
Farhat YA, Kim SH, Seyfferth AL, Zhang L, Neumann RB (2021) Altered arsenic availability, uptake, and allocation in rice under elevated temperature. Sci Total Environ 763:143049. https://doi.org/10.1016/j.scitotenv.2020.143049
Field CB, Barros V, Stocker TF, Dahe Q (2012) Managing the risks of extreme events and disasters to advance climate change adaptation: special report of the intergovernmental panel on climate change. Cambridge University Press
Food and Drug Administration [FDA] (2016) Inorganic Arsenic in Rice Cereals for Infants: Action Level Guidance for Industry - Draft Guidance. In: USDoHaH Services (ed). Center for Food Safety and Applied Nutrition, Rockville, MD, USA
GRiSP (2013) Rice Almanac. International Rice Research Institute, Los Baños
Gutiérrez JM, Jones RG, Narisma GT, Alves LM, Amjad M, Gorodetskaya IV, Grose M, Klutse NAB, Krakovska S, Li J, Martínez-Castro D, Mearns LO, Mernild SH, Ngo-Duc T, van den Hurk B, Yoon J-H (2021) 2021: Interactive Atlas. In: Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B (eds) Climate Change 2021: The Physical Science Basis Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change
Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Extremes 10:4–10. https://doi.org/10.1016/j.wace.2015.08.001
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp St 347:32
Huang B-Y, Zhao F-J, Wang P (2022) The relative contributions of root uptake and remobilization to the loading of Cd and As into rice grains: Implications in simultaneously controlling grain Cd and As accumulation using a segmented water management strategy. Environ Pollut 293:118497. https://doi.org/10.1016/j.envpol.2021.118497
Li RY, Stroud JL, Ma JF, McGrath SP, Zhao FJ (2009) Mitigation of Arsenic accumulation in rice with water management and silicon fertilization. Environ Sci Technol 43:3778–3783. https://doi.org/10.1021/es803643v
Li G, Sun G-X, Williams PN, Nunes L, Zhu Y-G (2011) Inorganic arsenic in Chinese food and its cancer risk. Environ Int 37:1219–1225. https://doi.org/10.1016/j.envint.2011.05.007
Linquist B, Ruark M (2011) Re-evaluating diagnostic phosphorus tests for rice systems based on soil phosphorus fractions and field level budgets. Agron J 103:501–508. https://doi.org/10.2134/agronj2010.0365
Liu J, Ma X, Wang M, Sun X (2011) Genotypic differences among rice cultivars in lead accumulation and translocation and the relation with grain Pb levels. Ecotoxicol Environ Saf 90:35–40. https://doi.org/10.1016/j.ecoenv.2012.12.007
Lu Y, Watanabe A, Kimura M (2002) Contribution of plant-derived carbon to soil microbial biomass dynamics in a paddy rice microcosm. Biol Fertil Soils 36:136–142. https://doi.org/10.1007/s00374-002-0504-2
Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci 105:9931–9935. https://doi.org/10.1073/pnas.0802361105
Ma R, Shen J, Wu J, Tang Z, Shen Q, Zhao F-J (2014) Impact of agronomic practices on arsenic accumulation and speciation in rice grain. Environ Pollut 194:217–223. https://doi.org/10.1016/j.envpol.2014.08.004
Meharg AA, Williams PN, Adomako E, Lawgali YY, Deacon C, Villada A, Cambell RCJ, Sun G, Zhu Y-G, Feldmann J, Raab A, Zhao F-J, Islam R, Hossain S, Yanai J (2009) Geographical variation in total and inorganic Arsenic content of polished (White) rice. Environ Sci Technol 43:1612–1617. https://doi.org/10.1021/es802612a
Mondal D, Polya DA (2008) Rice is a major exposure route for arsenic in Chakdaha block, Nadia district, West Bengal, India: A probabilistic risk assessment. Appl Geochem 23:2987–2998. https://doi.org/10.1016/j.apgeochem.2008.06.025
Muehe EM, Wang T, Kerl CF, Planer-Friedrich B, Fendorf S (2019) Rice production threatened by coupled stresses of climate and soil arsenic. Nat Commun 10:4985. https://doi.org/10.1038/s41467-019-12946-4
Müller V, Chavez-Capilla T, Feldmann J, Mestrot A (2022) Increasing temperature and flooding enhance arsenic release and biotransformations in Swiss soils. Sci Total Environ 838:156049. https://doi.org/10.1016/j.scitotenv.2022.156049
Neumann RB, Seyfferth AL, Teshera-Levye J, Ellingson J (2017) Soil warming increases Arsenic availability in the rice rhizosphere. Agric Environ Lett 2. https://doi.org/10.2134/ael2017.02.0006
Nishar A, Bader MKF, O’Gorman EJ, Deng J, Breen B, Leuzinger S (2017) Temperature effects on biomass and regeneration of vegetation in a geothermal area. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00249
Palta J, Watt M (2009) Chapter 13 - Vigorous crop root systems: form and function for improving the capture of water and nutrients. In: Sadras V, Calderini D (eds) Crop physiol. Academic Press, San Diego
Panaullah GM, Alam T, Hossain MB, Loeppert RH, Lauren JG, Meisner CA, Ahmed ZU, Duxbury JM (2008) Arsenic toxicity to rice (Oryza sativa L.) in Bangladesh. Plant Soil 317:31–39. https://doi.org/10.1007/s11104-008-9786-y
Public Health Alliance (2022) California Healthy Places Index: Extreme Heat Edition. Public Health Institute
Simmonds MB, Anders M, Adviento-Borbe MA, van Kessel C, McClung A, Linquist BA (2015) Seasonal methane and nitrous oxide emissions of several rice cultivars in direct-seeded systems. J Environ Qual 44:103–114. https://doi.org/10.2134/jeq2014.07.0286
Taylor GJ, Crowder AA (1983) Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am J Bot 70:1254–1257. https://doi.org/10.1002/j.1537-2197.1983.tb12474.x
The European Commision (2015) Commission Regulation (EU) 2015/1006 of 25 June 2015 amending Regulation (EC) No 1881/2006 as regards maximum levels of inorganic arsenic in foodstuffs. Official Journal of the European Union
Tu S, Ma L, Luongo T (2004) Root exudates and arsenic accumulation in arsenic hyperaccumulating Pteris vittata and non-hyperaccumulating Nephrolepis exaltata. Plant Soil 258:9–19. https://doi.org/10.1023/B:PLSO.0000016499.95722.16
Turpeinen R, Pantsar-Kallio M, Häggblom M, Kairesalo T (1999) Influence of microbes on the mobilization, toxicity and biomethylation of arsenic in soil. Sci Total Environ 236:173–180. https://doi.org/10.1016/S0048-9697(99)00269-7
U.S. EPA (1995) Integrated Risk Information System (IRIS) on Arsenic, inorganic, CASRN 7440–38-2. National Center for Environmental Assessment, Cincinnati, OH
Vezzani FM, Anderson C, Meenken E, Gillespie R, Peterson M, Beare MH (2018) The importance of plants to development and maintenance of soil structure, microbial communities and ecosystem functions. Soil Tillage Res 175:139–149. https://doi.org/10.1016/j.still.2017.09.002
Wang H, Inukai Y, Yamauchi A (2006) Root development and nutrient uptake. CRC Crit Rev Plant Sci 25:279–301. https://doi.org/10.1080/07352680600709917
Weber F-A, Hofacker AF, Voegelin A, Kretzschmar R (2010) Temperature dependence and coupling of iron and arsenic reduction and release during flooding of a contaminated soil. Environ Sci Technol 44:116–122. https://doi.org/10.1021/es902100h
Xu L, Polya DA, Li Q, Mondal D (2020) Association of low-level inorganic arsenic exposure from rice with age-standardized mortality risk of cardiovascular disease (CVD) in England and Wales. Sci Total Environ 743:140534. https://doi.org/10.1016/j.scitotenv.2020.140534
Yamaji N, Ma JF (2007) Spatial distribution and temporal variation of the rice silicon transporter Lsi1. Plant Physiol 143:1306–1313. https://doi.org/10.1104/pp.106.093005
Yamaji N, Ma JF (2011) Further characterization of a rice silicon efflux transporter, Lsi2. Soil Sci Plant Nutr 57:259–264. https://doi.org/10.1080/00380768.2011.565480
Yuan H, Wan Q, Huang Y, Chen Z, He X, Gustave W, Manzoor M, Liu X, Tang X, Ma LQ (2021) Warming facilitates microbial reduction and release of arsenic in flooded paddy soil and arsenic accumulation in rice grains. J Hazard Mater 408:124913. https://doi.org/10.1016/j.jhazmat.2020.124913
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794. https://doi.org/10.1111/j.1469-8137.2008.02716.x
Zheng MZ, Cai C, Hu Y, Sun GX, Williams PN, Cui HJ, Li G, Zhao FJ, Zhu YG (2011) Spatial distribution of arsenic and temporal variation of its concentration in rice. New Phytol 189:200–209. https://doi.org/10.1111/j.1469-8137.2010.03456.x