Research Progress on the Effects of OsNramp5 Mutation on Important Agronomic Traits in Rice

doi:10.16819/j.1001-7216.2022.220316

Abstract

Abstract:

Developing low-cadmium (Cd) rice cultivars is the most economical and effective way to solve the problem of “Cadmium Rice”. Previous studies have shown that OsNramp5 is the major transport gene for Cd uptake in rice. The functional deficiency of OsNramp5 leads to a significant decrease in the content of Cd in rice grains, and the uptake of manganese (Mn) is also affected. However, in previous studies on the effect of OsNramp5 variation on rice growth and development, the conclusions were inconsistent. The systematic understanding of the effects of OsNramp5 mutation on important agronomic traits in rice will promote the development of new rice cultivars with low-Cd and high-quality. This manuscript focuses on the effects of OsNramp5 mutation on the content of metal ions, growth and development, yield and quality of rice, so as to provide scientific guidance for the breeding of new rice cultivars with low Cd accumulation by OsNramp5 mutation.

Key words: rice, OsNramp5, cadmium, manganese, agronomic trait

摘要：

筛选和培育镉(Cd)低积累水稻品种是解决稻米镉污染问题最经济、有效的办法。现有研究表明OsNramp5是介导水稻Cd吸收最重要的基因，其功能缺失后，水稻籽粒Cd含量极显著下降，但同时会影响水稻必需元素锰(Mn)的吸收，而在前人关于OsNramp5变异影响水稻生长发育的研究中，结论并不一致。系统了解OsNramp5基因变异对水稻重要农艺性状的影响有助于推动低Cd优质水稻新品种的培育。本文重点对OsNramp5基因变异对水稻中金属离子的含量，水稻的生长发育、产量性状及米质的影响进行了综述，以期为利用OsNramp5基因突变选育低Cd积累水稻品种提供参考。

关键词: 水稻, OsNramp5, 镉, 锰, 农艺性状

LI Xiaoxiu, LÜ Qiming, YUAN Dingyang. Research Progress on the Effects of OsNramp5 Mutation on Important Agronomic Traits in Rice[J]. Chinese Journal OF Rice Science, 2022, 36(6): 562-571.

李小秀, 吕启明, 袁定阳. OsNramp5基因变异影响水稻重要农艺性状的研究进展[J]. 中国水稻科学, 2022, 36(6): 562-571.

Figures/Tables 3

References 63

[1]	Ye X X, Ma Y B, Sun B. Influence of soil type and genotype on Cd bioavailability and uptake by rice and implications for food safety[J]. Journal of Environmental Sciences, 2012, 24(9): 1647-1654.
[2]	Grant C A, Clarke J M, Duguid S, Chaney R L. Selection and breeding of plant cultivars to minimize cadmium accumulation[J]. The Science of the Total Environment, 2008, 390(2): 301-310.
[3]	Sui F Q, Chang J D, Tang Z, Liu W J, Huang X Y, Zhao F J. Nramp5 expression and functionality likely explain higher cadmium uptake in rice than in wheat and maize[J]. Plant and Soil, 2018, 433: 377-389.
[4]	Järup L, Akesson A. Current status of cadmium as an environmental health problem[J]. Toxicology and Applied Pharmacology, 2009, 238(3): 201-208.
[5]	Rikans L E, Yamano T. Mechanisms of cadmium- mediated acute hepatotoxicity[J]. Journal of Biochemical and Molecular Toxicology, 2000, 14(2): 110-117.
[6]	Åkesson A, Barregard L, Bergdahl I A, Nordberg G F, Nordberg M, Skerfving S. Non-renal effects and the risk assessment of environmental cadmium exposure[J]. Environmental Health Perspectives, 2014, 122(5): 431-438.
[7]	Li H, Luo N, Li Y W, Cai Q Y, Li, H Y, Mo C H, Wong M H. Cadmium in rice: Transport mechanisms, influencing factors, and minimizing measures[J]. Environmental Pollution, 2017, 224: 622-630.
[8]	Jiang M, Jiang J, Li S, Li M, Tan Y Y, Song S Y, Shu Q Y, Huang J Z. Glutamate alleviates cadmium toxicity in rice via suppressing cadmium uptake and translocation[J]. Journal of Hazardous Materials, 2020, 384: 121319.
[9]	Shan A, Kang K J, Xu H Z, Wu L, Lu M T, Lin Q, Pan M H, Wang G, He Z L, Yang X E. Cadmium accumulation in rice straws and derived biochars as affected by metal exposure, soil types and rice genotypes[J]. International Journal of Phytoremediation, 2021(1): 1-10.
[10]	Cattani I, Romani M, Boccelli R. Effect of cultivation practices on cadmium concentration in rice grain[J]. Agronomy for Sustainable Development, 2008, 28(2): 265-271.
[11]	Zhang Q, Li Z W, Huang B, Luo N L, Long L Z, Huang M, Zhai X Q, Zeng G M. Effect of land use pattern change from paddy soil to vegetable soil on the adsorption-desorption of cadmium by soil aggregates[J]. Environmental Science and Pollution Research International, 2017, 24(3): 2734-2743.
[12]	Mortensen L H, Rønn R, Vestergård M. Bioaccumulation of cadmium in soil organisms: With focus on wood ash application[J]. Ecotoxicology and Environmental Safety, 2018, 156: 452-462.
[13]	Yang Y, Li Y L, Wang M E, Chen W P, Dai Y T. Limestone dosage response of cadmium phytoavailability minimization in rice: A trade-off relationship between soil pH and amorphous manganese content[J]. Journal of Hazardous Materials, 2021, 403: 123664.
[14]	Shao J F, Fujii-Kashino M, Yamaji N, Fukuoka S, Shen R F, Ma J F. Isolation and characterization of a rice line with high Cd accumulation for potential use in phytoremediation[J]. Plant and Soil, 2017, 410(1): 357-368.
[15]	Acosta J A, Abbaspour A, Martínez G R, Martínez- Martínez S, Zornoza R, Gabarrón M, Faz A. Phytoremediation of mine tailings with Atriplex halimus and organic/inorganic amendments: A five-year field case study[J]. Chemosphere, 2018, 204: 71-78.
[16]	王林友, 竺朝娜, 王建军, 张礼霞, 金庆生, 石春海. 水稻镉、铅、砷低含量基因型的筛选[J]. 浙江农业学报, 2012, 24(1): 133-138.
	Wang L Y, Zhu C N, Wang J J, Zhang L X, Jin Q S, Shi C H. Screening for rice (Oryza sativa L.) genotypes with lower Cd, Pb and As contents[J]. Acta Agriculturae Zhejiangensis, 2012, 24(1): 133-138. (in Chinese with English abstract)
[17]	叶新新, 周艳丽, 孙波. 适于轻度Cd、As污染土壤种植的水稻品种筛选[J]. 农业环境科学学报, 2012, 31(6): 1082-1088.
	Ye X X, Zhou Y L, Sun B. Screening of suitable rice cultivars for the adaptation to lightly contaminated soil with Cd and As[J]. Journal of Agro-Environment Science, 2012, 31(6): 1082-1088. (in Chinese with English abstract)
[18]	Tang G H, Xie H J, Zhu M D, Xiao Y, Fu H R, Ling C Q, Yu Y H. Preliminary study on rice varieties with low cadmium accumulation by mixed planting[J]. Hunan Agricultural Sciences, 2018, 4: 17-20.
[19]	Shao J F, Xia J, Yamaji N, Shen R F, Ma J F. Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter[J]. Journal of Experimental Botany, 2018, 69(10): 2743-2752.
[20]	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. Mutation at different sites of metal transporter gene OsNramp5 affects Cd accumulation and related agronomic traits in rice (Oryza sativa L.)[J]. Frontiers in Plant Science, 2019, 10: 1081.
[21]	Chang J D, Huang S, Konishi N, Wang P, Chen J, Huang X Y, Ma J F, Zhao F J. Overexpression of the manganese/cadmium transporter OsNRAMP5 reduces cadmium accumulation in rice grain[J]. Journal of Experimental Botany, 2020, 71(18): 5705-5715.
[22]	Nevo Y, Nelson N. The NRAMP family of metal-ion transporters[J]. Biochimica et Biophysica Acta, 2006, 1763(7): 609-620.
[23]	Bozzi A T, Gaudet R. Molecular mechanism of NRAMP-family transition metal transport[J]. Journal of Molecular Biology, 2021, 433(16): 166991.
[24]	Petre B, Major I, Rouhier N, Duplessis S. Genome-wide analysis of eukaryote thaumatin-like proteins (TLPs) with an emphasis on poplar[J]. BMC Plant Biology, 2011, 11(1): 33.
[25]	Nelson N. Metal ion transporters and homeostasis[J]. The EMBO Journal, 1999, 18(16): 4361-4371.
[26]	Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, Obata H. Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni²⁺-transport abilities[J]. Plant Physiology and Biochemistry, 2005, 43(8): 793-801.
[27]	Oomen R J, Wu J, Lelièvre F, Blanchet S, Richaud P, Barbier-Brygoo H, Aarts M G, Thomine S. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens[J]. The New Phytologist, 2009, 181(3): 637-650.
[28]	Wei W, Chai T Y, Zhang Y X, Han L, Xu J, Guan Z Q. The Thlaspi caerulescens NRAMP homologue TcNRAMP3 is capable of divalent cation transport[J]. Molecular Biotechnology, 2009, 41(1): 15-21.
[29]	Xiao H H, Yin L P, Xu X F, Li T Z, Han Z H. The iron-regulated transporter, MbNRAMP1, isolated from Malus baccata is involved in Fe, Mn and Cd trafficking[J]. Annals of Botany, 2008, 102(6): 881-889.
[30]	Ishikawa S, Abe T, Kuramata M, Yamaguchi M, Ando T, Yamamoto T, Yano M. A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7[J]. Journal of Experimental Botany, 2010, 61(3): 923-934.
[31]	Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa N K. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice[J]. Journal of Experimental Botany, 2011, 62(14): 4843-4850.
[32]	Li Y, Li J J, Yu Y H, Dai X, Gong C Y, Gu D F, Xu E D, Liu Y H, Zou Y, Zhang P J, Chen X, Zhang W. The tonoplast-localized transporter OsNRAMP2 is involved in iron homeostasis and affects seed germination in rice[J]. Journal of Experimental Botany, 2021, 72(13): 4839-4852.
[33]	Yamaji N, Sasaki A, Xia J X, Yokosho K, Ma J F. A node-based switch for preferential distribution of manganese in rice[J]. Nature Communications, 2013, 4: 2442.
[34]	Yang M, Zhang W, Dong H X, Zhang Y Y, Lü K, Wang D J, Lian X M. OsNRAMP3 is a vascular bundles-specific manganese transporter that is responsible for manganese distribution in rice[J]. PLoS ONE, 2013, 8(12): e83990.
[35]	Xia J, Yamaji N, Kasai T, Ma J F. Plasma membrane-localized transporter for aluminum in rice[J]. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(43): 18381-18385.
[36]	Li J Y, Liu J, Dong D, Jia X, McCouch S R, Kochian L V. Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance[J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(17): 6503-6508.
[37]	Peris-Peris C, Serra-Cardona A, Sánchez-Sanuy F, Campo S, Ariño J, San Segundo B. Two NRAMP6 isoforms function as iron and manganese transporters and contribute to disease resistance in rice[J]. Molecular Plant-Microbe Interactions, 2017, 30(5): 385-398.
[38]	吴天昊, 李曜魁, 孙远涛, 董家瑜, 莫伊凡, 唐丽, 赵炳然. 水稻OsNRAMP7基因的克隆、表达及生物信息学分析[J]. 分子植物育种, 2021, 19(7): 2103-2110.
	Wu T H, Li Y K, Sun Y T, Dong J Y, Mo Y F, Tang L, Zhao B R. Cloning, expression and bioinformatical analysis of OsNAMP7 gene in rice[J]. Molecular Plant Breeding, 2021, 19(7): 2103-2110. (in Chinese with English abstract)
[39]	Sperotto R A, Boff T, Duarte G L, Santos L S, Grusak M A, Fett J P. Identification of putative target genes to manipulate Fe and Zn concentrations in rice grains[J]. Journal of Plant Physiology, 2010, 167(17): 1500-1506.
[40]	Sasaki A, Yamaji N, Yokosho K, Ma J F. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice[J]. The Plant Cell, 2012, 24(5): 2155-2167.
[41]	Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa N K, Nakanishi H. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(47): 19166-19171.
[42]	Ishimaru Y, Bashir K, Nakanishi H, Nishizawa N K. OsNRAMP5, a major player for constitutive iron and manganese uptake in rice[J]. Plant Signaling & Behavior, 2012, 7(7): 763-766.
[43]	Yang M, Zhang Y Y, Zhang L J, Hu J T, Zhang X, Lu K, Dong H X, Wang D J, Zhao F J, Huang C F, Lian X M. OsNRAMP5 contributes to manganese translocation and distribution in rice shoots[J]. Journal of Experimental Botany, 2014, 65(17): 4849-4961.
[44]	Uraguchi S, Fujiwara T. Cadmium transport and tolerance in rice: Perspectives for reducing grain cadmium accumulation[J]. Rice, 2012, 5(1): 5.
[45]	杨猛. 水稻NRAMP家族基因在Mn和Cd转运中的功能研究[D]. 武汉: 华中农业大学, 2014.
	Yang M. Functional Analysis of Rice NRAMP Genes in Mn and Cd Transport[D]. Wuhan: Huazhong Agricultural University, 2014. (in Chinese with English abstract)
[46]	Tang L, Mao B G, Li Y K, Lü Q M, Zhang L P, Chen C Y, He H J, Wang W P, Zeng X F, Shao Y, Pan Y L, Hu Y Y, Peng Y, Fu X Q, Li H Q, Xia S T, Zhao B R. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield[J]. Scientific Reports, 2017, 7(1): 14438.
[47]	Yang C H, Zhang Y, Huang C F. Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9- mediated editing of OsNRAMP5[J]. Journal of Integrative Agriculture, 2019, 18: 688-697.
[48]	Liu S M, Jiang J, Liu Y, Meng J, Xu S L, Tan Y Y, Li Y F, Shu Q Y, Huang J Z. Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice[J]. Rice Science, 2019, 26(2): 88-97.
[49]	龙起樟, 黄永兰, 唐秀英, 王会民, 芦明, 袁林峰, 万建林. 利用CRISPR/Cas9敲除OsNramp5基因创制低镉籼稻[J]. 中国水稻科学, 2019, 33(5): 407-420.
	Long Q Z, Huang Y L, Tang X Y, Wang H M, Lu M, Yuan L F, Wan J L. Creation of Low-Cd-accumulating indica rice by disruption of OsNramp5 gene via CRISPR/Cas9[J]. Chinese Journal of Rice Science, 2019, 33(5): 407-420. (in Chinese with English abstract)
[50]	胡黎明, 彭彦, 郑文杰, 周凯, 毛慧, 唐丽, 毛毕刚. 利用CRISPR/Cas9技术创制镉低积累香型水稻[J]. 杂交水稻, 2021, 36(6): 77-83.
	Hu L M, Peng Y, Zheng W J, Zhou K, Mao H, Tang L, Mao B G. Using CRISPR/Cas9 technology to create low cadmium accumulation and aromatic rice[J]. Hybrid Rice, 2021, 36(6): 77-83. (in Chinese with English abstract)
[51]	Tanaka N, Nishida S, Kamiya T, Fujiwara T. Large-scale profiling of brown rice ionome in an ethyl methanesulphonate-mutagenized hitomebore population and identification of high- and low-cadmium lines[J]. Plant and Soil, 2016, 407(1): 109-117.
[52]	Cao Z Z, Lin X Y, Yang Y J, Guan M Y, Xu P, Chen M X. Gene identification and transcriptome analysis of low cadmium accumulation rice mutant (lcd1) in response to cadmium stress using MutMap and RNA-seq[J]. BMC Plant Biology, 2019, 19(1): 250.
[53]	Tang L, Dong J, Qu M, Lü Q, Zhang L, Peng C, Hu Y, Li Y, Ji Z, Mao B, Peng Y, Shao Y, Zhao B. Knockout of OsNRAMP5 enhances rice tolerance to cadmium toxicity in response to varying external cadmium concentrations via distinct mechanisms[J]. The Science of the Total Environment, 2022, 832: 155006.
[54]	Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa N K. Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport[J]. Scientific Reports, 2012, 2: 286.
[55]	刘松梅. 水稻镉运输基因OsLCT1和OsNramp5的特征与突变分析[D]. 杭州: 浙江大学, 2019.
	Liu S H. Characterization and mutational analysis of cadmium transport genes OsLCTl and OsNramp5 in rice[D]. Hangzhou: Zhejiang University, 2019. (in Chinese with English abstract)
[56]	Tsunemitsu Y, Yamaji N, Ma J F, Kato S I, Iwasaki K, Ueno D. Rice reduces Mn uptake in response to Mn stress[J]. Plant Signaling & Behavior, 2018, 13(1): 2476-2491.
[57]	Chang J D, Huang S, Yamaji N, Zhang W W, Ma J F, Zhao F J. OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice[J]. Plant, Cell & Environment, 2020, 43(10): 2476-2491.
[58]	董家瑜, 吴天昊, 孙远涛, 何含杰, 李曜魁, 彭彦, 冀中英, 孟前程, 赵炳然, 唐丽. 不同锰浓度环境下OsNRAMP5突变对水稻耐热性和主要经济性状的影响[J]. 杂交水稻, 2021, 36(2): 79-88.
	Dong J Y, Wu T H, Sun Y T, He H J, Li Y K, Peng Y, Ji Z Y, Meng Q C, Zhao B R, Tang L. Effects of OsNRAMP5 mutation on heat tolerance and main economic traits of rice under the conditions of different manganese concentration[J]. Hybrid Rice, 2021, 36(2): 79-88. (in Chinese with English abstract)
[59]	Sasaki A, Yamaji N, Ma J F. Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice[J]. Journal of Experimental Botany, 2014, 65(20): 6013-6021.
[60]	Lu C, Zhang L X, Tang Z, Huang X Y, Ma J F, Zhao F J. Producing cadmium-free Indica rice by overexpressing OsHMA3[J]. Environment International, 2019, 126: 619-626.
[61]	Lü Q M, Li W G, Sun Z Z, Ouyang N, Jing X, He Q, Wu J, Zheng J K, Zheng J T, Tang S Q, Zhu R S, Tian Y, Duan M J, Tan Y N, Yu D, Sheng X B, Sun X W, Jia G F, Gao H Z, Zeng Q, Li Y F, Tang L, Xu Q S, Zhao B R, Huang Z Y, Lu H F, Li N, Zhao J, Zhu L H, Li D, Yuan L P, Yuan D Y. Resequencing of 1,143 indica rice accessions reveals important genetic variations and different heterosis patterns[J]. Nature Communications, 2020, 11(1): 4778.
[62]	王天抗, 李懿星, 宋书锋, 傅岳峰, 余应弘, 柏连阳, 李莉. 水稻籽粒镉低积累资源挖掘及其新材料创制[J]. 杂交水稻, 2021, 36(1): 68-74.
	Wang T K, Li Y X, Song S F, Fu Y F, Yu Y H, Bai L Y, Li L. Excavation of rice resources with low cadmium accumulation in grains and development of new materials[J]. Hybrid Rice, 2021, 36(1): 68-74. (in Chinese with English abstract)
[63]	韶也, 彭彦, 毛毕刚, 余丽霞, 唐丽, 李曜魁, 胡远艺, 张丹, 袁智成, 罗武中, 彭选明, 李文建, 周利斌, 柏连阳, 赵炳然. M_1TDS技术及镉低积累杂交水稻亲本创制与组合选育[J]. 杂交水稻, 2022, 37(1): 1-11.
	Shao Y, Peng Y, Mao B G, Yu L X, Tang L, Li Y K, Hu Y Y, Zhang D, Yuan Z C, Luo W Z, Peng X M, Li W J, Zhou L B, Bai L Y, Zhao B R. M_1TDS technology and creation of low-cadmium accumulation parents for hybrid rice breeding[J]. Hybrid Rice, 2022, 37(1): 1-11. (in Chinese with English abstract)

基因符号 Gene symbol	组织表达 Tissue expression	亚细胞定位 Subcellular localization	金属转运功能 Metal transport function	参考文献 Reference
OsNramp1	根、叶 Root, leaf	质膜Plasma membrane	Cd	[30,31]
OsNramp2	地上部 Aboveground part	液泡膜 Tonoplast	Fe	[32]
OsNramp3	维管束 Vascular bundle	质膜Plasma membrane	Mn	[33,34]
OsNramp4	根 Root	质膜Plasma membrane	Al	[35,36]
OsNramp5	根 Root	质膜Plasma membrane	Cd, Mn, Fe	[40⇓⇓-43]
OsNramp6	不详 Unavailable	质膜Plasma membrane	Fe, Mn	[37]
OsNramp7	根、茎、幼穗 Root, culm, young panicle	不详 Unavailable	Fe, Zn	[38,39]

基因符号 Gene symbol	组织表达 Tissue expression	亚细胞定位 Subcellular localization	金属转运功能 Metal transport function	参考文献 Reference
OsNramp1	根、叶 Root, leaf	质膜Plasma membrane	Cd	[30,31]
OsNramp2	地上部 Aboveground part	液泡膜 Tonoplast	Fe	[32]
OsNramp3	维管束 Vascular bundle	质膜Plasma membrane	Mn	[33,34]
OsNramp4	根 Root	质膜Plasma membrane	Al	[35,36]
OsNramp5	根 Root	质膜Plasma membrane	Cd, Mn, Fe	[40⇓⇓-43]
OsNramp6	不详 Unavailable	质膜Plasma membrane	Fe, Mn	[37]
OsNramp7	根、茎、幼穗 Root, culm, young panicle	不详 Unavailable	Fe, Zn	[38,39]

变异位置 Mutation site	变异来源Mutation method	遗传背景Genetic background	变异类型 Mutation type	籽粒Cd、Mn含量Contents of Cd and Mn in grains	其他金属含量 Other metal content	产量及其他性状 Yield and other traits	参考文献Reference
第1外显子	CRISPR/Cas9技术	南粳46、淮稻5号	1 bp插入	Cd、Mn显著下降	对Fe无显著影响	产量、株高、每穗粒数、结实率均显著降低，穗数增加	[47]
			17 bp插入	Cd、Mn显著下降	对Fe无显著影响	产量、株高、每穗粒数、结实率均显著降低	[47]
			11 bp插入	Cd、Mn显著下降	对Fe无显著影响	产量、株高、每穗粒数、结实率均显著降低	[47]
		中花11	4 bp缺失	Cd、Mn显著下降	—	生长严重受阻，根及地上部干质量显著降低	[57]
第2外显子	CRISPR/Cas9技术	黄华占	1 bp插入	Cd、Mn显著下降	对Fe、Zn无显著影响	产量、每穗粒数、结实率、秸秆产量均显著降低，米质变劣，分蘖数增加	[20]
第6外显子	CRISPR/Cas9技术	黄华占	2 bp插入	Cd、Mn显著下降	对Fe、Zn无显著影响	产量、每穗粒数、结实率、秸秆产量均显著降低，米质变劣	[20]
第7外显子	CRISPR/Cas9技术	锡稻1号	1 bp插入	Cd显著下降	—	产量、其他性状无显著影响	[48]
	EMS诱变	9311	SNP变异	Cd显著下降	对Fe、Zn、Cu无显著影响	其他性状无显著影响	[52]
第8外显子	EMS诱变	Hitomebore	SNP变异	Cd、Mn显著下降	—	产量、其他性状无显著影响	[51]
第9外显子	碳离子束辐射诱变	越光	1 bp缺失	Cd<0.05 mg/kg， Mn显著下降	对Fe、Zn、Cu无显著影响	产量、其他性状无显著影响	[41]
	CRISPR/Cas9技术	华占	3 bp缺失+ 1 bp插入	Cd<0.05 mg/kg， Mn极显著下降	对Cu、Zn无显著影响， Fe显著上升	产量、其他性状无显著影响	[46]
			5 bp缺失	Cd<0.05 mg/kg， Mn极显著下降	对Cu、Zn无显著影响， Fe显著上升	产量、其他性状无显著影响	[46]
		锡稻1号	33 bp缺失	Cd显著下降	—	减产44.3%，生长严重受阻，株高降低	[48]
		黄华占	1 bp插入	均显著下降	对Fe、Zn无显著影响	产量、每穗粒数、结实率、秸秆生物量均显著降低	[20]
		中花11	2 bp缺失+ 1 bp插入	—	—	产量、千粒重极显著降低，米质变劣	[58]
		中花11	5 bp缺失+ 1 bp插入	—	—	产量、千粒重极显著降低，米质变劣	[58]
第10外显子	碳离子束辐射诱变	越光	433 bp插入	Cd<0.05 mg/kg，Mn显著下降	对Fe、Zn、Cu 无显著影响	产量、其他性状无显著影响	[41]
	CRISPR/Cas9技术	华占、五丰B、五山丝苗、中早35	1-3 bp缺失+ 1 bp插入	Cd、Mn显著下降	对Fe、Zn、Cu、Ca、 As、Se无显著影响	减产6.9%，株高、结实率、千粒重小幅降低，有效分蘖略微增加	[49]
第5内含子	T-DNA插入	中花11	大片段插入	—	对K、Ca、Mg、Zn、 Cu无显著影响	生长受阻，叶片变黄	[43]
第8内含子	碳离子束辐射诱变	隆臻36S、华恢8612	18 bp缺失	Cd、Mn显著下降	—	产量、其他性状无显著影响	[63]
第10内含子	碳离子束辐射诱变	隆臻36S、华恢8612	3 bp缺失	Cd、Mn显著下降	—	产量、其他性状无显著影响	[63]
第12内含子	T-DNA插入	中花11	大片段插入	Cd、Mn显著下降	对Fe、Zn、Cu无显著影响	减产89%，生长受阻，叶片严重失绿	[40]
全基因缺失	碳离子束辐射诱变	越光	227 kb缺失	Cd<0.05 mg/kg， Mn显著下降	对Fe、Zn无显著影响， Cu显著上升	产量显著降低，抽穗早，株型小，穗数多，但秸秆产量低	[41]
全基因缺失	⁶⁰Co辐射诱变	粤泰B	408 kb缺失	Cd显著下降	—	—	[61-62]

变异位置 Mutation site	变异来源Mutation method	遗传背景Genetic background	变异类型 Mutation type	籽粒Cd、Mn含量Contents of Cd and Mn in grains	其他金属含量 Other metal content	产量及其他性状 Yield and other traits	参考文献Reference
第1外显子	CRISPR/Cas9技术	南粳46、淮稻5号	1 bp插入	Cd、Mn显著下降	对Fe无显著影响	产量、株高、每穗粒数、结实率均显著降低，穗数增加	[47]
			17 bp插入	Cd、Mn显著下降	对Fe无显著影响	产量、株高、每穗粒数、结实率均显著降低	[47]
			11 bp插入	Cd、Mn显著下降	对Fe无显著影响	产量、株高、每穗粒数、结实率均显著降低	[47]
		中花11	4 bp缺失	Cd、Mn显著下降	—	生长严重受阻，根及地上部干质量显著降低	[57]
第2外显子	CRISPR/Cas9技术	黄华占	1 bp插入	Cd、Mn显著下降	对Fe、Zn无显著影响	产量、每穗粒数、结实率、秸秆产量均显著降低，米质变劣，分蘖数增加	[20]
第6外显子	CRISPR/Cas9技术	黄华占	2 bp插入	Cd、Mn显著下降	对Fe、Zn无显著影响	产量、每穗粒数、结实率、秸秆产量均显著降低，米质变劣	[20]
第7外显子	CRISPR/Cas9技术	锡稻1号	1 bp插入	Cd显著下降	—	产量、其他性状无显著影响	[48]
	EMS诱变	9311	SNP变异	Cd显著下降	对Fe、Zn、Cu无显著影响	其他性状无显著影响	[52]
第8外显子	EMS诱变	Hitomebore	SNP变异	Cd、Mn显著下降	—	产量、其他性状无显著影响	[51]
第9外显子	碳离子束辐射诱变	越光	1 bp缺失	Cd<0.05 mg/kg， Mn显著下降	对Fe、Zn、Cu无显著影响	产量、其他性状无显著影响	[41]
	CRISPR/Cas9技术	华占	3 bp缺失+ 1 bp插入	Cd<0.05 mg/kg， Mn极显著下降	对Cu、Zn无显著影响， Fe显著上升	产量、其他性状无显著影响	[46]
			5 bp缺失	Cd<0.05 mg/kg， Mn极显著下降	对Cu、Zn无显著影响， Fe显著上升	产量、其他性状无显著影响	[46]
		锡稻1号	33 bp缺失	Cd显著下降	—	减产44.3%，生长严重受阻，株高降低	[48]
		黄华占	1 bp插入	均显著下降	对Fe、Zn无显著影响	产量、每穗粒数、结实率、秸秆生物量均显著降低	[20]
		中花11	2 bp缺失+ 1 bp插入	—	—	产量、千粒重极显著降低，米质变劣	[58]
		中花11	5 bp缺失+ 1 bp插入	—	—	产量、千粒重极显著降低，米质变劣	[58]
第10外显子	碳离子束辐射诱变	越光	433 bp插入	Cd<0.05 mg/kg，Mn显著下降	对Fe、Zn、Cu 无显著影响	产量、其他性状无显著影响	[41]
	CRISPR/Cas9技术	华占、五丰B、五山丝苗、中早35	1-3 bp缺失+ 1 bp插入	Cd、Mn显著下降	对Fe、Zn、Cu、Ca、 As、Se无显著影响	减产6.9%，株高、结实率、千粒重小幅降低，有效分蘖略微增加	[49]
第5内含子	T-DNA插入	中花11	大片段插入	—	对K、Ca、Mg、Zn、 Cu无显著影响	生长受阻，叶片变黄	[43]
第8内含子	碳离子束辐射诱变	隆臻36S、华恢8612	18 bp缺失	Cd、Mn显著下降	—	产量、其他性状无显著影响	[63]
第10内含子	碳离子束辐射诱变	隆臻36S、华恢8612	3 bp缺失	Cd、Mn显著下降	—	产量、其他性状无显著影响	[63]
第12内含子	T-DNA插入	中花11	大片段插入	Cd、Mn显著下降	对Fe、Zn、Cu无显著影响	减产89%，生长受阻，叶片严重失绿	[40]
全基因缺失	碳离子束辐射诱变	越光	227 kb缺失	Cd<0.05 mg/kg， Mn显著下降	对Fe、Zn无显著影响， Cu显著上升	产量显著降低，抽穗早，株型小，穗数多，但秸秆产量低	[41]
全基因缺失	⁶⁰Co辐射诱变	粤泰B	408 kb缺失	Cd显著下降	—	—	[61-62]