脱落酸通过调控水稻对镉的转运和细胞壁的阻隔降低镉积累

doi:10.1016/j.jia.2025.02.010

摘要/Abstract

摘要：

镉影响水稻生长，其随食物链迁移进入人体严重威胁人类的健康，因此，研究水稻对镉的响应和调控过程显得尤为重要。本研究通过转录组分析发现大量脱落酸相关的基因响应镉胁迫，后续通过施加外源脱落酸可以显著降低水稻地上部和根部的镉含量。不仅如此，外源脱落酸可能通过提高抗坏血酸过氧化物酶活性以及降低过氧化氢水平缓解镉对水稻的毒害。后续研究表明，脱落酸可以通过调控水稻对镉的转运和细胞壁的阻隔作用，减少水稻植株的镉积累。进一步的，脱落酸信号因子OsABI5突变可导致水稻地上部镉含量提高。此外，在水稻灌浆期叶面喷施脱落酸能显著降低水稻籽粒中的镉积累，并主要通过降低水稻对镉的吸收、抑制镉从根部向地上部转运以及抑制镉从叶片向籽粒的转运实现。本研究不仅揭示了脱落酸在调节水稻镉胁迫响应中的潜在机制，也为应对农田镉污染提供了参考。

Abstract:

Uptake of cadmium (Cd) by rice plants and its subsequent movement through food chains pose a notable risk to the health of both plants and humans. Consequently, it is crucial to uncover the fundamental mechanisms involved in this process. Through transcriptome analysis, we found that numerous abscisic acid (ABA)-related genes respond to Cd stress. Exogenous application of ABA significantly reduced Cd accumulation in the shoots and roots of rice plants. The increased ascorbate peroxidase (APX) enzyme activity, decreased H₂O₂ content, and elevated Cd tolerance index collectively suggest that ABA may mitigate the toxicity of Cd in rice plants. Further study revealed that exogenous ABA reduced Cd accumulation by regulating Cd transport and cell wall sequestration. Consistently, mutation of the ABA signaling factor OsABI5 resulted in a significant increase in Cd accumulation in shoots. Moreover, foliar spraying of ABA during the grain filling stage significantly reduced Cd accumulation in rice grains, which was attributed mainly to decreased Cd uptake and the inhibition of Cd transportation from roots to shoots and from leaves to grains. These findings elucidate the underlying mechanisms of the ABA-mediated response to Cd stress in rice and provide a practical reference for coping with Cd pollution in farmlands.

Key words: rice , Cd accumulation , Cd toxicity , abscisic acid , cell wall

. 脱落酸通过调控水稻对镉的转运和细胞壁的阻隔降低镉积累[J]. Journal of Integrative Agriculture, DOI: 10.1016/j.jia.2025.02.010.

Zhijun Xu, Jiashi Peng, Yanlei Fu, Jing Zhao, Yan Peng, Bohan Liu, Xujun Hu, Yuchuan Liu, Meijuan Duan, Nenghui Ye, Zhenxie Yi, Shuan Meng. Abscisic acid reduces Cd accumulation by regulating Cd transport and cell wall sequestration in rice[J]. Journal of Integrative Agriculture, DOI: 10.1016/j.jia.2025.02.010.

参考文献

Bali S, Jamwal V L, Kohli S K, Kaur P, Tejpal R, Bhalla V, Ohri P, Gandhi S G, Bhardwaj R, Al-Huqail A A, Siddiqui M H, Ali H M, Ahmad P. 2019. Jasmonic acid application triggers detoxification of lead (Pb) toxicity in tomato through the modifications of secondary metabolites and gene expression. Chemosphere, 235, 734-748.

Bezrukova M V, Fatkhutdinova R A, Lubyanova A R, Murzabaev A R, Fedyaev V V, Shakirova F M. 2011. Lectin involvement in the development of wheat tolerance to cadmium toxicity. Russian Journal of Plant Physiology, 58, 1048-1054.

Chang J D, Huang S, Yamaji N, Zhang W, Ma J F, Zhao F J. 2020. OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice. Plant Cell and Environment, 43, 2476-2491.

Chen J, Wu X, Song J, Xing G, Liang L, Yin Q, Guo A, Cui J. 2021. Transcriptomic and physiological comparsion of the short-term responses of two Oryza sativa L. varieties to cadmium. Environmental and Experimental Botany, 181, 104292.

Chu C, Huang R, Liu L, Tang G, Xiao J, Yoo H, Yuan M. 2022. The rice heavy-metal transporter OsNRAMP1 regulates disease resistance by modulating ROS homoeostasis. Plant Cell and Environment, 45, 1109-1126.

Fan S K, Fang X Z, Guan M Y, Ye Y Q, Lin X Y, Du S T, Jin C W. 2014. Exogenous abscisic acid application decreases cadmium accumulation in Arabidopsis plants, which is associated with the inhibition of IRT1-mediated cadmium uptake. Frontiers in Plant Science, 5, 721.

Guerriero G, Sergeant K, Hausman J F. 2014. Wood biosynthesis and typologies: A molecular rhapsody. Tree Physiology, 34, 839-855.

Gumińska N, Plecha M, Walkiewicz H, Halakuc P, Zakrys B, Milanowski R. 2018. Culture purification and DNA extraction procedures suitable for next-generation sequencing of euglenids. Journal of Applied Phycology, 30, 3541-3549.

Han Y, Wang S, Zhao N, Deng S, Zhao C, Li N, Sun J, Zhao R, Yi H, Shen X, Chen S. 2016. Exogenous abscisic acid alleviates cadmium toxicity by restricting Cd²⁺ influx in Populus euphratica cells. Journal of Plant Growth Regulation, 35, 827-837.

He L, Li J. 2022. Integrated transcriptome and physiological analysis of rice seedlings reveals different cadmium response mechanisms between indica and japonica varieties. Environmental and Experimental Botany, 204, 105097.

He X L, Fan S K, Zhu J, Guan M Y, Liu X X, Zhang Y S, Jin C W. 2017. Iron supply prevents Cd uptake in Arabidopsis by inhibiting IRT1 expression and favoring competition between Fe and Cd uptake. Plant and Soil, 416, 453-462.

Hsu Y T, Kao C H. 2003. Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Cell and Environment, 26, 867-874.

Kim D, Langmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12, 357-360.

Kuang L, Yan T, Gao F, Tang W, Wu D. 2024. Multi-omics analysis reveals differential molecular responses to cadmium toxicity in rice root tip and mature zone. Journal of Hazardous Materials, 462, 132758.

Kulsum P G P S, Khanam R, Das S, Nayak A K, Tack F M G, Meers E, Vithanage M, Shahid M, Kumar A, Chakraborty S, Bhattacharya T, Biswas J K. 2023. A state-of-the-art review on cadmium uptake, toxicity, and tolerance in rice: From physiological response to remediation process. Environmental Research, 220, 115098.

Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T. 2005. Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant Journal, 44, 939-949.

Leng Y, Li Y, Ma Y H, He L F, Li S W. 2021. Abscisic acid modulates differential physiological and biochemical responses of roots, stems, and leaves in mung bean seedlings to cadmium stress. Environmental Science and Pollution Research, 28, 6030-6043.

Li B, Wang S, You X, Wen Z, Huang G, Huang C, Li Q, Chen K, Zhao Y, Gu M, Li X, Wei Y, Qin Y. 2023. Effect of foliar spraying of gibberellins and brassinolide on cadmium accumulation in rice. Toxics, 11, 364.

Li Y, Qi X. 2023. Tryptophan pretreatment adjusts transcriptome and metabolome profiles to alleviate cadmium toxicity in Arabidopsis. Journal of Hazardous Materials, 452, 131226.

Li Y, Zhang S, Bao Q, Chu Y, Sun H, Huang Y. 2022. Jasmonic acid alleviates cadmium toxicity through regulating the antioxidant response and enhancing the chelation of cadmium in rice (Oryza sativa L.). Environmental Pollution, 304, 119178.

Lin J H, Xu Z J, Peng J S, Zhao J, Zhang G B, Xie J, Yi Z X, Zhang J H, Gong J M, Ye N H, Meng S. 2019. OsProT1 and OsProT3 function to mediate proline- and γ-aminobutyric acid-specific transport in yeast and are differentially expressed in rice (Oryza sativa L.). Rice, 12, 79.

Lin Z, Li Y, Wang Y, Liu X, Ma L, Zhang Z, Mu C, Zhang Y, Peng L, Xie S, Song C P, Shi H, Zhu J K, Wang P. 2021. Initiation and amplification of SnRK2 activation in abscisic acid signaling. Nature Communications, 12, 2456.

Liu Y S, Tao Y, Yang X Z, Liu Y N, Shen R F, Zhu X F. 2022. Gibberellic acid alleviates cadmium toxicity in rice by regulating NO accumulation and cell wall fixation capacity of cadmium. Journal of Hazardous Materials, 439, 129597.

Lu G, Gao C, Zheng X, Han B. 2009. Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta, 229, 605-615.

Lu C, Zhang L, Tang Z, Huang X Y, Ma J F, Zhao F J. 2019. Producing cadmium-free indica rice by overexpressing OsHMA3. Environment International, 126, 619-626.

Luo J S, Huang J, Zeng D L, Peng J S, Zhang G B, Ma H L, Guan Y, Yi H Y, Fu Y L, Han B, Lin H X, Qian Q, Gong J M. 2018. A defensin-like protein drives cadmium efflux and allocation in rice. Nature Communications, 9, 645.

Luo Q, Bai B, Xie Y, Yao D, Zhang D, Chen Z, Zhuang W, Deng Q, Xiao Y, Wu J. 2022. Effects of Cd uptake, translocation and redistribution in different hybrid rice varieties on grain Cd concentration. Ecotoxicology and Environmental Safety, 240, 113683.

Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H. 2011. OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytologist, 189, 190-199.

Muhammad S, Ulhassan Z, Munir R, Yasin MU, Islam F, Zhang K, Chen W, Jan M, Afzal M, Muhammad A, Hannan F, Zhou W. 2024. Nanosilica and salicylic acid synergistically regulate cadmium toxicity in rice. Environmental Pollution, 364, 125331.

Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa N K. 2006. Iron deficiency enhances cadmium uptake and translocation mediated by the Fe²⁺ transporters OsIRT1 and OsIRT2 in rice. Soil Science and Plant Nutrition, 52, 464-469.

Pan J, Guan M, Xu P, Chen M, Cao Z. 2021. Salicylic acid reduces cadmium (Cd) accumulation in rice (Oryza sativa L.) by regulating root cell wall composition via nitric oxide signaling. Science of the Total Environment, 797, 149202.

Pan W, You Y, Shentu J L, Weng Y N, Wang S T, Xu Q R, Liu H J, Du S T. 2020. Abscisic acid (ABA)-importing transporter 1 (AIT1) contributes to the inhibition of Cd accumulation via exogenous ABA application in Arabidopsis. Journal of Hazardous Materials, 391, 122189

Panda P, Nath S, Chanu T T, Sharma G D, Panda S K. 2011. Cadmium stress-induced oxidative stress and role of nitric oxide in rice (Oryza sativa L.). Acta Physiologiae Plantarum, 33, 1737-1747.

Parrotta L, Guerriero G, Sergeant K, Cal G, Hausman J F. 2015. Target or barrier? The cell wall of early- and later-diverging plants vs. cadmium toxicity: Differences in the response mechanisms. Frontiers in Plant Science, 6, 133.

Peng J S, Wang Y J, Ding G, Ma H L, Zhang Y J, Gong J M. 2017. A pivotal role of cell wall in cadmium accumulation in the Crassulaceae hyperaccumulator Sedum plumbizincicola. Molecular Plant, 10, 771-774.

Sasaki A, Yamaji N, Ma J F. 2014. Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. Journal of Experimental Botany, 65, 6013-6021.

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, 2155-2167.

Skubacz A, Daszkowska-Golec A, Szarejko I. 2016. The role and regulation of ABI5 (ABA-Insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Frontiers in Plant Science, 7, 1884.

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. Journal of Experimental Botany, 62, 4843-4850.

Tang L, Dong J, Qu M, Lv Q, Zhang L, Peng C, Hu Y, Li Y, Ji Z, Mao B, Peng Y, Shao Y, Zhao B. 2022. Knockout of OsNRAMP5 enhances rice tolerance to cadmium toxicity in response to varying external cadmium concentrations via distinct mechanisms. Science of the Total Environment, 832, 155006.

Tao J, Lu L. 2022. Advances in genes-encoding transporters for cadmium uptake, translocation, and accumulation in plants. Toxics, 10, 411.

Tian S, Liang S, Qiao K, Wang F, Zhang Y, Chai T. 2019. Co-expression of multiple heavy metal transporters changes the translocation, accumulation, and potential oxidative stress of Cd and Zn in rice (Oryza sativa). Journal of Hazardous Materials, 380, 120853.

Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma J F. 2010. Gene limiting cadmium accumulation in rice. Proceedings of the National Academy of Sciences of the United States of America, 107, 16500-16505.

Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T. 2011. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proceedings of the National Academy of Sciences of the United States of America, 108, 20959-20964.

Wang F, Tan H, Huang L, Cai C, Ding Y, Bao H, Chen Z, Zhu C. 2021. Application of exogenous salicylic acid reduces Cd toxicity and Cd accumulation in rice. Ecotoxicology and Environmental Safety, 207, 111198.

Wang Y, Wu F, Lin Q, Sheng P, Wu Z, Jin X, Chen W, Li S, Luo S, Duan E, Wang J, Ma W, Ren Y, Cheng Z, Zhang X, Lei C, Guo X, Wang H, Zhu S, Wan J. 2023. A regulatory loop establishes the link between the circadian clock and abscisic acid signaling in rice. Plant Physiology, 191, 1857-1870.

Wu H, Tong J, Jiang X, Wang J, Zhang H, Luo Y, Pang J, Shi J. 2024. More effective than direct contact: Nano hydroxyapatite pre-treatment regulates the growth and Cd uptake of rice (Oryza sativa L.) seedlings. Journal of Hazardous Materials, 463, 132889.

Yan H, Zhang H, Hao S, Wang L, Xu W, Mi M, Luo Y, He Z. 2023. Cadmium contamination in food crops: Risk assessment and control in smart age. Critical Reviews in Environmental Science and Technology, 53, 1643-1661,

Yang Y, Xiong J, Chen R, Fu G, Chen T, Tao L. 2016. Excessive nitrate enhances cadmium (Cd) uptake by up-regulating the expression of OsIRT1 in rice (Oryza sativa). Environmental and Experimental Botany, 122, 141-149.

You Y, Wang Y, Zhang S, Sun X, Liu H, Guo E Y, Du S. 2022. Different pathways for exogenous ABA-mediated down-regulation of cadmium accumulation in plants under different iron supplies. Journal of Hazardous Materials, 440, 129769.

Yu E, Wang W, Yamaji N, Fukuoka S, Che J, Ueno D, Ando T, Deng F, Hori K, Yano M, Shen R F, Ma J F. 2022. Duplication of a manganese/cadmium transporter gene reduces cadmium accumulation in rice grain. Nature Food, 3, 597-607.

Yu X, Yang L, Fan C, Hu J, Zheng Y, Wang Z, Liu Y, Xiao X, Yang L, Lei T, Jiang M, Jiang B, Pan Y, Li X, Gao S, Zhou Y. 2023. Abscisic acid (ABA) alleviates cadmium toxicity by enhancing the adsorption of cadmium to root cell walls and inducing antioxidant defense system of Cosmos bipinnatus. Ecotoxicology and Environmental Safety, 261, 115101.

Zhao F Y, Wang K, Zhang S Y, Ren J, Liu T, Wang X. 2014. Crosstalk between ABA, auxin, MAPK signaling, and the cell cycle in cadmium-stressed rice seedlings. Acta Physiologiae Plantarum, 36, 1879-1892.

Zong W, Tang N, Yang J, Peng L, Ma S, Xu Y, Li G, Xiong L. 2016. Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought-resistance-related genes. Plant Physiology, 171, 2810-2825.

Zou M, Guan Y, Ren H, Zhang F, Chen F. 2008. A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Molecular Biology, 66, 675-683.

Zou M, Zhou S, Zhou Y, Jia Z, Guo T, Wang J. 2021. Cadmium pollution of soil-rice ecosystems in rice cultivation dominated regions in China: A review. Environmental Pollution, 280, 116965.