Appropriate Supply of Ammonium Nitrogen and Ammonium Nitrate Reduces Cadmium Content in Rice Seedlings by Inhibiting Cadmium Uptake and Transport
Received date: 2023-12-04
Accepted date: 2024-02-05
Online published: 2024-10-11
Reasonable nitrogen (N) application is a promising strategy for reducing crop cadmium (Cd) toxicity. However, the specific form of N and the required amount that affect Cd tolerance and accumulation in rice remain unclear. This study explored the influence of different N-fertilizer forms (NH4NO3, NH4Cl, and KNO3) and dosages on Cd tolerance and uptake in Cd-stressed N-sensitive and N-insensitive indica rice accessions. The results indicated that the Cd tolerance of N-sensitive indica accessions is more robust than that of N-insensitive ones. Furthermore, the shoot Cd content and Cd translocation rate in both N-sensitive and N-insensitive indica accessions decreased with an appropriate supply of NH4NO3 and NH4Cl, whereas they were comparable or slightly increased with increased KNO3. Unfortunately, we did not find significant and regular differences in Cd accumulation or translocation between N-sensitive and N-insensitive rice accessions. Consistent with the reduction of shoot Cd content, the addition of NH4NO3 and NH4Cl also inhibited the instantaneous root Cd2+ uptake. The expression changes of Cd transport-related genes under different N forms and dosages suggested that the decreased shoot Cd content, caused by the increased supply of NH4NO3 and NH4Cl, is likely achieved by reducing the transcription of OsNRAMP1 and OsIRT1. In summary, our findings reveal that an appropriate supply of NH4NO3 and NH4Cl could reduce Cd uptake and transport in rice seedlings, suggesting that rational N management could reduce the Cd risk in rice production.
Key words： Oryza sativa; cadmium; nitrogen; ammonium nitrate; ammonium chloride
Hu Yunchao, Yan Tiancai, Gao Zhenyu, Wang Tiankang, Lu Xueli, Yang Long, Shen Lan, Zhang Qiang, Hu Jiang, Ren Deyong, Zhang Guangheng, Zhu Li, Li Li, Zeng Dali, Qian Qian, Li Qing . Appropriate Supply of Ammonium Nitrogen and Ammonium Nitrate Reduces Cadmium Content in Rice Seedlings by Inhibiting Cadmium Uptake and Transport[J]. Rice Science, 2024 , 31(5) : 587 -602 . DOI: 10.1016/j.rsci.2024.02.007
| [1] | Adeosun A A, Price A H, Norton G J. 2023. Cadmium tolerance and accumulation in wild rice species. Rice Sci, 30(3): 181-185. |
| [2] | ?kesson A, Barregard L, Bergdahl I A, Nordberg G F, Nordberg M, Skerfving S. 2014. Non-renal effects and the risk assessment of environmental cadmium exposure. Environ Health Perspect, 122(5): 431-438. |
| [3] | Anders S, Pyl P T, Huber W. 2015. HTSeq: A python framework to work with high-throughput sequencing data. Bioinformatics, 31(2): 166-169. |
| [4] | Bai Z Q, Zhu L, Chang H X, Wu J W. 2021a. Enhancement of cadmium accumulation in sweet sorghum as affected by nitrate. Plant Biol, 23(1): 66-73. |
| [5] | Bai Z Q, Li D, Zhu L, Tang X Y, Wang Y F, Mao R J, Wu J W. 2021b. Nitrate increases cadmium accumulation in sweet sorghum for improving phytoextraction efficiency rather than ammonium. Front Plant Sci, 12: 643116. |
| [6] | Chang J D, Huang S, Yamaji N, Zhang W W, Ma J F, Zhao F J. 2020. OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice. Plant Cell Environ, 43(10): 2476-2491. |
| [7] | Chanh T T, Tsutsumi M, Kurihara K. 1981. Comparative study on the response of indica and japonica rice plants to ammonium and nitrate nitrogen. Soil Sci Plant Nutr, 27(1): 83-92. |
| [8] | Chen A L, Liu T, Deng Y, Xiao R, Zhang T, Wang Y, Yang Y H, Lakshmanan P, Shi X J, Zhang F S, Chen X P. 2023. Nitrate-dependent suberization regulates cadmium uptake and accumulation in maize. Sci Total Environ, 878: 162848. |
| [9] | Chen J G, Zou W L, Meng L J, Fan X R, Xu G H, Ye G Y. 2019. Advances in the uptake and transport mechanisms and QTLs mapping of cadmium in rice. Int J Mol Sci, 20(14): 3417. |
| [10] | Cheng M M, Wang P, Kopittke P M, Wang A N, Sale P W G, Tang C X. 2016. Cadmium accumulation is enhanced by ammonium compared to nitrate in two hyperaccumulators, without affecting speciation. J Exp Bot, 67(17): 5041-5050. |
| [11] | Cheng M M, Wang A N, Tang C X. 2017. Ammonium-based fertilizers enhance Cd accumulation in Carpobrotus rossii grown in two soils differing in pH. Chemosphere, 188: 689-696. |
| [12] | Clemens S, Aarts M G M, Thomine S, Verbruggen N. 2013. Plant science: The key to preventing slow cadmium poisoning. Trends Plant Sci, 18(2): 92-99. |
| [13] | Cramer M D, Lewis O A M. 1993. The influence of NO3- and NH4+ nutrition on the carbon and nitrogen partitioning characteristics of wheat (Triticum aestivum L.) and maize (Zea mays L.) plants. Plant Soil, 154(2): 289-300. |
| [14] | Ding Y F, Ye Y Y, Jiang Z H, Wang Y, Zhu C. 2016. MicroRNA390 is involved in cadmium tolerance and accumulation in rice. Front Plant Sci, 7: 235. |
| [15] | Du Q, Chen M X, Zhou R, Chao Z Y, Zhu Z W, Shao G S, Wang G M. 2009. Cd toxicity and accumulation in rice plants vary with soil nitrogen status and their genotypic difference can be partly attributed to nitrogen uptake capacity. Rice Sci, 16(4): 283-291. |
| [16] | Eriksson J E. 1990. Effects of nitrogen-containing fertilizers on solubility and plant uptake of cadmium. Water Air Soil Pollut, 49(3): 355-368. |
| [17] | Guo S, Zhou Y, Shen Q, Zhang F. 2007. Effect of ammonium and nitrate nutrition on some physiological processes in higher plants-growth, photosynthesis, photorespiration, and water relations. Plant Biol, 9(1): 21-29. |
| [18] | Hasan S A, Fariduddin Q, Ali B, Hayat S, Ahmad A. 2009. Cadmium: Toxicity and tolerance in plants. J Environ Biol, 30(2): 165-174. |
| [19] | Hassan M J, Wang F, Ali S, Zhang G P. 2005. Toxic effect of cadmium on rice as affected by nitrogen fertilizer form. Plant Soil, 277(1): 359-365. |
| [20] | Hassan M J, Shafi M, Zhang G P, Zhu Z J, Qaisar M. 2008a. The growth and some physiological responses of rice to Cd toxicity as affected by nitrogen form. Plant Growth Regul, 54(2): 125-132. |
| [21] | Hassan M J, Zhang G P, Zhu Z J. 2008b. Influence of cadmium toxicity on plant growth and nitrogen uptake in rice as affected by nitrogen form. J Plant Nutr, 31(2): 251-262. |
| [22] | Hu P J, Yin Y G, Ishikawa S, Suzui N, Kawachi N, Fujimaki S, Igura M, Yuan C, Huang J X, Li Z, Makino T, Luo Y M, Christie P, Wu L H. 2013. Nitrate facilitates cadmium uptake, transport and accumulation in the hyperaccumulator Sedum plumbizincicola. Environ Sci Pollut Res Int, 20(9): 6306-6316. |
| [23] | Jalloh M A, Chen J H, Zhen F R, Zhang G P. 2009. Effect of different N fertilizer forms on antioxidant capacity and grain yield of rice growing under Cd stress. J Hazard Mater, 162(2/3): 1081-1085. |
| [24] | J?rup L, Akesson A. 2009. Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol, 238(3): 201-208. |
| [25] | Jiang L L, Wu L, Wang Y, Xu Q, Xu Z J, Chen W F. 2022. Research progress on the divergence and genetic basis of agronomic traits in Xian and Geng rice. Crop J, 10(4): 924-931. |
| [26] | Kim D, Langmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nat Methods, 12(4): 357-360. |
| [27] | Larsson J?nsson E H, Asp H. 2013. Effects of pH and nitrogen on cadmium uptake in potato. Biol Plant, 57(4): 788-792. |
| [28] | Lee S, An G. 2009. Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ, 32(4): 408-416. |
| [29] | Li Q, Lu X L, Wang C J, Shen L, Dai L P, He J L, Yang L, Li P Y, Hong Y F, Zhang Q, Dong G J, Hu J, Zhang G H, Ren D Y, Gao Z Y, Guo L B, Qian Q, Zhu L, Zeng D L. 2022. Genome-wide association study and transcriptome analysis reveal new QTL and candidate genes for nitrogen-deficiency tolerance in rice. Crop J, 10(4): 942-951. |
| [30] | Lin Y L, Chao Y Y, Huang W D, Kao C H. 2011. Effect of nitrogen deficiency on antioxidant status and Cd toxicity in rice seedlings. Plant Growth Regul, 64(3): 263-273. |
| [31] | Liu Z Y, Zhu C S, Jiang Y, Tian Y L, Yu J, An H Z, Tang W J, Sun J, Tang J P, Chen G M, Zhai H Q, Wang C M, Wan J M. 2016. Association mapping and genetic dissection of nitrogen use efficiency-related traits in rice (Oryza sativa L.). Funct Integr Genomic, 16(3): 323-333. |
| [32] | Luo B F, Du S T, Lu K X, Liu W J, Lin X Y, Jin C W. 2012. Iron uptake system mediates nitrate-facilitated cadmium accumulation in tomato (Solanum lycopersicum) plants. J Exp Bot, 63(8): 3127-3136. |
| [33] | Maier N A, McLaughlin M J, Heap M, Butt M, Smart M K. 2002. Effect of nitrogen source and calcitic lime on soil pH and potato yield, leaf chemical composition, and tuber cadmium concentrations. J Plant Nutr, 25(3): 523-544. |
| [34] | Morishita T, Fumoto N, Yoshizawa T, Kagawa K. 1987. Varietal differences in cadmium levels of rice grains of japonica, indica, Javanica, and hybrid varieties produced in the same plot of a field. Soil Sci Plant Nutr, 33(4): 629-637. |
| [35] | Nawrot T S, Staessen J A, Roels H A, Munters E, Cuypers A, Richart T, Ruttens A, Smeets K, Clijsters H, Vangronsveld J. 2010. Cadmium exposure in the population: From health risks to strategies of prevention. Biometals, 23(5): 769-782. |
| [36] | Nordberg G F. 2009. Historical perspectives on cadmium toxicology. Toxicol Appl Pharmacol, 238(3): 192-200. |
| [37] | Rizwan M, Ali S, Adrees M, Rizvi H, Zia-Ur-Rehman M, Hannan F, Qayyum M F, Hafeez F, Ok Y S. 2016. Cadmium stress in rice: Toxic effects, tolerance mechanisms, and management: A critical review. Environ Sci Pollut Res Int, 23(18): 17859-17879. |
| [38] | Sasaki A, Yamaji N, Yokosho K, Ma J F. 2012. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell, 24(5): 2155-2167. |
| [39] | Satarug S, Garrett S H, Sens M A, Sens D A. 2010. Cadmium, environmental exposure, and health outcomes. Environ Health Perspect, 118(2): 182-190. |
| [40] | Song Y, Wang Y, Mao W F, Sui H X, Yong L, Yang D J, Jiang D G, Zhang L, Gong Y Y. 2017. Dietary cadmium exposure assessment among the Chinese population. PLoS One, 12(5): e0177978. |
| [41] | Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa N K. 2011. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot, 62(14): 4843-4850. |
| [42] | Tang W J, Ye J, Yao X M, Zhao P Z, Xuan W, Tian Y L, Zhang Y Y, Xu S, An H Z, Chen G M, Yu J, Wu W, Ge Y W, Liu X L, Li J, Zhang H Z, Zhao Y Q, Yang B, Jiang X Z, Peng C, Zhou C, Terzaghi W, Wang C M, Wan J M. 2019. Genome-wide associated study identifies NAC42-activated nitrate transporter conferring high nitrogen use efficiency in rice. Nat Commun, 10(1): 5279. |
| [43] | Tsadilas C D, Karaivazoglou N A, Tsotsolis N C, Stamatiadis S, Samaras V. 2005. Cadmium uptake by tobacco as affected by liming, N form, and year of cultivation. Environ Pollut, 134(2): 239-246. |
| [44] | Uraguchi S, Fujiwara T. 2012. Cadmium transport and tolerance in rice: Perspectives for reducing grain cadmium accumulation. Rice, 5(1): 5. |
| [45] | Vazquez A, Recalde L, Cabrera A, Groppa M D, Benavides M P. 2020. Does nitrogen source influence cadmium distribution in Arabidopsis plants? Ecotoxicol Environ Saf, 191: 110163. |
| [46] | Wang J F, Li W L, Li Q S, Wang L L, He T, Wang F P, Xu Z M. 2021. Nitrogen fertilizer management affects remobilization of the immobilized cadmium in soil and its accumulation in crop tissues. Environ Sci Pollut Res Int, 28(24): 31640-31652. |
| [47] | Wang T K, Li Y X, Fu Y F, Xie H J, Song S F, Qiu M D, Wen J, Chen M W, Chen G, Tian Y, Li C X, Yuan D Y, Wang J L, Li L. 2019. Mutation at different sites of metal transporter gene OsNramp5 affects Cd accumulation and related agronomic traits in rice (Oryza sativa L.). Front Plant Sci, 10: 1081. |
| [48] | W?ngstrand H, Eriksson J, ?born I. 2007. Cadmium concentration in winter wheat as affected by nitrogen fertilization. Eur J Agron, 26(3): 209-214. |
| [49] | Wu Z C, Zhang W J, Xu S J, Shi H Z, Wen D, Huang Y D, Peng L J, Deng T H B, Du R Y, Li F R, Wang X, Wang F H. 2018. Increasing ammonium nutrition as a strategy for inhibition of cadmium uptake and xylem transport in rice (Oryza sativa L.) exposed to cadmium stress. Environ Exp Bot, 155: 734-741. |
| [50] | Xie H L, Jiang R F, Zhang F S, McGrath S P, Zhao F J. 2009. Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant Soil, 318(1): 205-215. |
| [51] | Yan H L, Xu W X, Xie J Y, Gao Y W, Wu L L, Sun L, Feng L, Chen X, Zhang T, Dai C H, Li T, Lin X N, Zhang Z Y, Wang X Q, Li F M, Zhu X Y, Li J J, Li Z C, Chen C Y, Ma M, Zhang H L, He Z Y. 2019. Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nat Commun, 10(1): 2562. |
| [52] | Yang Y J, Xiong J, Chen R J, Fu G F, Chen T T, Tao L X. 2016. Excessive nitrate enhances cadmium (Cd) uptake by up-regulating the expression of OsIRT1 in rice (Oryza sativa). Environ Exp Bot, 122: 141-149. |
| [53] | Zaccheo P, Crippa L, Di Muzio Pasta V. 2006. Ammonium nutrition as a strategy for cadmium mobilisation in the rhizosphere of sunflower. Plant Soil, 283(1): 43-56. |
| [54] | Zeng X Y, Zou D S, Wang A D, Zhou Y Y, Liu Y H, Li Z H, Liu F, Wang H, Zeng Q R, Xiao Z H. 2020. Remediation of cadmium- contaminated soils using Brassica napus: Effect of nitrogen fertilizers. J Environ Manage, 255: 109885. |
| [55] | Zhang J L, Zhu Y C, Yu L J, Yang M, Zou X, Yin C X, Lin Y J. 2022. Research advances in cadmium uptake, transport and resistance in rice (Oryza sativa L.). Cells, 11(3): 569. |
| [56] | Zhang L D, Liu X, Wei M Y, Guo Z J, Zhao Z Z, Gao C H, Li J, Xu J X, Shen Z J, Zheng H L. 2022. Ammonium has stronger Cd detoxification ability than nitrate by reducing Cd influx and increasing Cd fixation in Solanum nigrum L. J Hazard Mater, 425: 127947. |
| [57] | Zhang Z H, Chu C C. 2020. Nitrogen-use divergence between indica and japonica rice: Variation at nitrate assimilation. Mol Plant, 13(1): 6-7. |
| [58] | Zhao J L, Yang W, Zhang S H, Yang T F, Liu Q, Dong J F, Fu H, Mao X X, Liu B. 2018. Genome-wide association study and candidate gene analysis of rice cadmium accumulation in grain in a diverse rice collection. Rice, 11(1): 61. |
| [59] | Zhu C Q, Cao X C, Zhu L F, Hu W J, Hu A Y, Bai Z G, Zhong C, Sun L M, Liang Q D, Huang J, Yang S X, Zhang J H, Jin Q Y. 2018. Ammonium mitigates Cd toxicity in rice (Oryza sativa) via putrescine-dependent alterations of cell wall composition. Plant Physiol Biochem, 132: 189-201. |
| [60] | Zhu D F, Zhang Y P, Chen H Z, Xiang J, Zhang Y K. 2015. Innovation and practice of high-yield rice cultivation technology in China. Sci Agric Sin, 48(17): 3404-3414. (in Chinese with English abstract) |
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