Genome-wide Identification and Expression Pattern Analysis of WRI1 Gene Family in Erythropalum scandens

doi:10.13560/j.cnki.biotech.bull.1985.2024-1212

Abstract

Abstract:

Objective Identification of the WRI1 transcription factor in Erythropalum scandens provides a foundation for further investigation into its role in lipid biosynthesis. Method The whole genome data of E. scandens were used to identify the WRI1 transcription factors in E. scandens by bioinformatics methods. Based on transcriptome data, the expression patterns of WRI1 in different tissues of E. scandens were analyzed. Result A total of 17 WRI1proteins (EsWRI1-1-EsWRI1-17) containing two AP2 conserved domains were identified in E. scandens. The number of amino acids was 359-776, and the average molecular weight was 56 kD. Most of them were acidic and unstably hydrophilic proteins. Subcellular localization showed that it was mostly located in the nucleus, and 17 EsWRI1s members were unevenly distributed on 8 chromosomes. The results of protein sequence phylogenetic analysis divided 17 WRI1 proteins into nine subfamilies (Group 1-Group 9). Among them, Group 3 members were closely related to Arabidopsis thaliana and Glycine max, and EsWRI1-10 was closely related to A. thaliana. The promoter analysis of the EsWRI1s gene family showed that it contained more motifs related to biotic and abiotic stress, plant response to hormone,and plant growth and development, among which the growth and development-related elements were the most. The analysis of gene expression patterns showed that the expressions of EsWRI1-10, EsWRI1-14 and EsWRI1-16 genes in immature kernels were higher than those in other tissues, among which EsWRI1-10 gene played a major role in the formation of kernels, EsWRI1-11, EsWRI1-17 and EsWRI1-7 were highly expressed in different tissues of E. scandens. The RT-qPCR validation was consistent with the transcriptome data. Conclusion A total of 17 WRI1 genes are identified. Their encoded proteins possess favorable thermal stability and hydrophilicity and are predicted to be mainly located in the cell nucleus. The EsWRI1s gene family shares high homology with that of A. thaliana, G. max and M. oleifera. Specific genes are expressed specifically in immature seed kernels, implying their significant roles in kernel growth and development and potentially in lipid synthesis of E. scandens.

Key words: Erythropalum scandens, WRI1 transcription factor, gene family, oil, medicine and food homologous plants, oleic acid, expression pattern analysis

HUANG Shi-yu, TIAN Shan-shan, YANG Tian-wei, GAO Man-rong, ZHANG Shang-wen. Genome-wide Identification and Expression Pattern Analysis of WRI1 Gene Family in Erythropalum scandens[J]. Biotechnology Bulletin, 2025, 41(8): 242-254.

Figures/Tables 10

References 41

[1]	黄诗宇, 杨天为, 张向军, 等. 不同品种赤苍藤种仁营养成分及潜在应用价值分析 [J]. 中国油脂, 2025, 50(6): 105-110.
	Huang SY, Yang TW, Zhang XJ, et al. Analysis of nutritional components and potential application value of seed kernels of Erythropalum scandens of different varieties [J]. China Oils and Fats, 2025, 50(6): 105-110.
[2]	隆卫革, 黎素平, 安家成, 等. 森林蔬菜赤苍藤营养分析与评价 [J]. 食品研究与开发, 2017, 38(24): 124-127.
	Long WG, Li SP, An JC, et al. Analysis and evaluation of nutritional components in Erythropalum scandens blume [J]. Food Res Dev, 2017, 38(24): 124-127.
[3]	中国科学院中国植物志编辑委员会编. 中国植物志 [M]. 北京: 科学出版社, 2004.
	Editorial Committee of Chinese Academy of Sciences. Chinese Flora [M]. Beijing: Science Press, 2004.
[4]	张军. 木本油料作物在土壤改良和生态恢复中的效益分析 [J]. 农村科学实验, 2024(7): 37-39.
	Zhang J. Benefit analysis of woody oil crops in soil improvement and ecological restoration [J]. Rural Sci Exp, 2024(7): 37-39.
[5]	熊旭东, 于安民, 孙蕊, 等. 高值木本油料植物蒜头果的资源发掘与利用 [J]. 中国野生植物资源, 2023, 42(1): 86-92.
	Xiong XD, Yu AM, Sun R, et al. Exploitation and utilization of MOC, A high-value oil plant [J]. Chin Wild Plant Resour, 2023, 42(1): 86-92.
[6]	杨一山, 唐健民, 孙菲菲, 等. 蒜头果不同部位的营养成分分析 [J]. 广西植物, 2023, 43(3): 515-526.
	Yang YS, Tang JM, Sun FF, et al. Analysis of nutritional components in different parts of Malania oleifera [J]. Guihaia, 2023, 43(3): 515-526.
[7]	孙小雨, 郭娟, 张丽, 等. 蒜头果种子萌发过程中油脂的变化 [J]. 热带农业科技, 2024, 47(3): 46-52.
	Sun XY, Guo J, Zhang L, et al. Changes in oil during seed germination of Malania oleifera [J]. Trop Agric Sci Technol, 2024, 47(3): 46-52.
[8]	许久恒. 文冠果与蒜头果神经酸合成及油脂转录调控的转录组研究 [D]. 北京: 北京林业大学, 2021.
	Xu JH. Transcriptome study on the synthesis of nervonic acid and the regulation of oil transcription in Xanthoceras sorbifolia Bunge and Malania oleifera Bunge [D]. Beijing: Beijing Forestry University, 2021.
[9]	黄和, 任波, 孙小曼. ω-3多不饱和脂肪酸健康机制及应用研究进展 [J]. 食品科学技术学报, 2024, 42(5): 1-12.
	Huang H, Ren B, Sun XM. Research progress on health mechanism and application of omega-3 polyunsaturated fatty acids. [J]. Journal of Food Science and Technology, 2024, 42(5): 1-12.
[10]	Baud S, Mendoza MS, To A, et al. WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis [J]. Plant J, 2007, 50(5): 825-838.
[11]	Ma W, Kong Q, Arondel V, et al. Wrinkled1, a ubiquitous regulator in oil accumulating tissues from Arabidopsis embryos to oil palm mesocarp [J]. PLoS One, 2013, 8(7): e68887.
[12]	Cernac A, Benning C. WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis [J]. Plant J, 2004, 40(4): 575-585.
[13]	Focks N, Benning C. wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism [J]. Plant Physiol, 1998, 118(1): 91-101.
[14]	Marchive C, Nikovics K, To A, et al. Transcriptional regulation of fatty acid production in higher plants: Molecular bases and biotechnological outcomes [J]. Eur J Lipid Sci Technol, 2014, 116(10): 1332-1343.
[15]	Ruuska SA, Girke T, Benning C, et al. Contrapuntal networks of gene expression during Arabidopsis seed filling [J]. Plant Cell, 2002, 14(6): 1191-1206.
[16]	Zhai ZY, Keereetaweep J, Liu H, et al. The role of sugar signaling in regulating plant fatty acid synthesis [J]. Front Plant Sci, 2021, 12: 643843.
[17]	金龙飞, 周丽霞, 曹红星, 等. WRI1调控植物油脂合成的研究进展 [J]. 中国油料作物学报, 2022, 44(4): 687-698.
	Jin LF, Zhou LX, Cao HX, et al. Progress on WRI1 regulation of plant oil biosynthesis [J]. Chin J Oil Crop Sci, 2022, 44(4): 687-698.
[18]	Ma W, Kong Q, Grix M, et al. Deletion of a C-terminal intrinsically disordered region of WRINKLED1 affects its stability and enhances oil accumulation in Arabidopsis [J]. Plant J, 2015, 83(5): 864-874.
[19]	叶专, 李小丽, 普永权. 转基因WRI1稻米的脂肪酸基因表达效果 [J]. 中国食品卫生杂志, 2015, 27(4): 367-371.
	Ye Z, Li XL, Pu YQ. The transgenic rice WRI1 fatty acids gene expression effect [J]. Chin J Food Hyg, 2015, 27(4): 367-371.
[20]	鲁亚萍. 花生Oleosin启动子和Ara h1启动子功能鉴定及转录因子WRI1基因的in silico分析 [D]. 泰安: 山东农业大学, 2012.
	Lu YP. Functional identification of oleosin promoter and Ara h1 promoter in peanut and in silico analysis of transcription factor WRI1 gene [D]. Tai'an: Shandong Agricultural University, 2012.
[21]	王莉莉. 甘蓝型油菜AP2亚家族转录因子及植物中WRI1的基因组学分析 [D]. 杨凌: 西北农林科技大学, 2016.
	Wang LL. Transcription factors of AP2 subfamily in Brassica napus and genomic analysis of WRI1 in plants [D]. Yangling: Northwest A & F University, 2016.
[22]	邵宇鹏, 杨明明, 包格格, 等. 大豆GmWRI1a基因启动子克隆及其功能分析 [J]. 中国油料作物学报, 2019, 41(4): 517-523.
	Shao YP, Yang MM, Bao GG, et al. Cloning and functional analysis of soybean GmWRI1a promoter [J]. Chin J Oil Crop Sci, 2019, 41(4): 517-523.
[23]	杨红丽, 向旭敏, 曹东, 等. 转录因子GmWRI1b促进大豆油脂合成的功能研究 [J/OL]. 中国油料作物学报, 2024. .
	Yang HL, Xiang XM, Cao D, et al. Function of transcription factor GmWRI1b promoting soybean oil synthesis [J/OL]. Chin J Oil Crop Sci, 2024. .
[24]	冯小燕, 王其凤, 岳柯昕, 等. 紫苏AP2基因家族PfWRI1促进植物种子油脂积累 [J]. 中国生物化学与分子生物学报, 2024, 40(8): 1161-1172.
	Feng XY, Wang QF, Yue KX, et al. Perilla AP2 gene family PfWRI1 promotes oil accumulation in plant seeds [J]. Chinese Journal of Biochemistry and Molecular Biology, 2024, 40(8): 1161-1172.
[25]	Adhikari ND, Bates PD, Browse J. WRINKLED1 rescues feedback inhibition of fatty acid synthesis in hydroxylase-expressing seeds [J]. Plant Physiol, 2016, 171(1): 179-191.
[26]	李佳奇, 任滢蓥, 刘沙, 等. 红花CtWRI1基因克隆与功能分析 [J]. 农业生物技术学报, 2024, 32(5): 1061-1070.
	Li JQ, Ren YY, Liu S, et al. Cloning and functional analysis of CtWRI1 gene from safflower (Carthamus tinctorius) [J]. J Agric Biotechnol, 2024, 32(5): 1061-1070.
[27]	李一沛. ‘凤丹’转录因子基因PoWRI1克隆及其牡丹籽油合成功能鉴定 [D]. 北京: 北京林业大学, 2021.
	Li YP. Cloning of transcription factor gene PoWRI1 from 'Fengdan' and identification of its synthetic function of peony seed oil [D]. Beijing: Beijing Forestry University, 2021.
[28]	万薇, 武学霞, 焦琬尧, 等. 藜麦WRI1基因家族鉴定与分析 [J]. 分子植物育种, 2025, 23(9): 2826-2834.
	Wan W, Wu XX, Jiao WY, et al. Identification and analysis of WRI1 gene family in quinoa [J]. Mol Plant Breed, 2025, 23(9): 2826-2834.
[29]	孙金波, 石素华, 杨利, 等. 花生WRI1基因家族的全基因组与表达谱分析 [J]. 花生学报, 2020, 49(1): 9-18.
	Sun JB, Shi SH, Yang L, et al. Genome-wide analysis of WRI1 gene family and their expression profiles in peanut [J]. J Peanut Sci, 2020, 49(1): 9-18.
[30]	刘克鑫, 杨宸, 王俊丽, 等. 亚麻荠WRI1转录因子基因家族的生物信息学分析 [J/OL]. 分子植物育种, 2023. .
	Liu KX, Yang C, Wang JL, et al. Bioinformatics analysis of WRI1 in Camelina sativa [J/OL]. Mol Plant Breed, 2023. .
[31]	王巍杰, 吴丹, 王涛. 大豆转录因子WRI1基因的生物信息学分析 [J]. 湖北农业科学, 2016, 55(13): 3482-3485, 3489.
	Wang WJ, Wu D, Wang T. Bioinformatics analysis of WRI1 transcription factors in soybean [J]. Hubei Agric Sci, 2016, 55(13): 3482-3485, 3489.
[32]	马倩, 李景滨, 阮成江, 等. 沙棘WRI1转录因子基因的生物信息学分析 [J]. 湖北农业科学, 2016, 55(22): 5972-5975, 5981.
	Ma Q, Li JB, Ruan CJ, et al. Bioinformatics analysis of WRI1 gene in Hippophae rhamnoides [J]. Hubei Agric Sci, 2016, 55(22): 5972-5975, 5981.
[33]	An D, Kim H, Ju S, et al. Expression of Camelina WRINKLED1 isoforms rescue the seed phenotype of the Arabidopsis wri1 mutant and increase the triacylglycerol content in tobacco leaves [J]. Front Plant Sci, 2017, 8: 34.
[34]	王贵芳, 王文茹, 张淑辉, 等. 核桃油脂合成转录因子JrWRI1基因的克隆及生物信息学分析 [J]. 山东农业科学, 2019, 51(2): 1-6.
	Wang GF, Wang WR, Zhang SH, et al. Cloning and bioinformatics analysis of transcription factor JrWRI1 gene related with lipids synthesis of walnut [J]. Shandong Agric Sci, 2019, 51(2): 1-6.
[35]	Nakano T, Suzuki K, Fujimura T, et al. Genome-wide analysis of the ERF gene family in Arabidopsis and rice [J]. Plant Physiol, 2006, 140(2): 411-432.
[36]	杨先友, 黄有军, 张通, 等. 拟南芥转录激活因子AtWRI1研究进展 [J]. 生物技术通报, 2016, 32(6): 13-18.
	Yang XY, Huang YJ, Zhang T, et al. Advances on transcriptional activator AtWRI1 of Arabidopsis [J]. Biotechnol Bull, 2016, 32(6): 13-18.
[37]	陈贝贝. 大豆二酰甘油酰基转移酶(DGAT)和转录因子WRINKLED1 (WRI1) 功能研究 [D]. 武汉: 华中农业大学, 2019.
	Chen BB. Study on the function of soybean diacylglycerol acyltransferase (DGAT) and transcription factor WRINKLED1(WRI1) [D]. Wuhan: Huazhong Agricultural University, 2019.
[38]	王月, 雷培, 季喜梅, 等. 蓖麻RcWRI1基因表达分析及生物信息学分析 [J]. 分子植物育种, 2018, 16(5): 1461-1467.
	Wang Y, Lei P, Ji XM, et al. Expression analysis and bioinformatics analysis of RcWRI1 gene in Castor [J]. Mol Plant Breed, 2018, 16(5): 1461-1467.
[39]	李鑫, 王正明, 薛伟, 等. 棉花中一个新型转录因子GhWRI1的表达特征与功能分析 [J]. 生物技术通报, 2013, 29(6): 80-86.
	Li X, Wang ZM, Xue W, et al. Identification and characterization of a novel gene, GhWRI1, encoding an AP2-type transcription factor in Gossypium hirsutum [J]. Biotechnol Bull, 2013, 29(6): 80-86.
[40]	莫宗明, 黄银珊, 谭长强. 广西蒜头果可持续发展关键技术措施 [J]. 防护林科技, 2024(3): 83-85.
	Mo ZM, Huang YS, Tan CQ. Key technical measures for sustainable development of Malania oleifera in Guangxi [J]. Prot For Sci Technol, 2024(3): 83-85.
[41]	韦贵元, 党桂兰, 胡琦敏, 等. 赤苍藤开发利用研究进展 [J]. 海峡药学, 2023, 35(2): 27-30.
	Wei GY, Dang GL, Hu QM, et al. Research progress and utilization of Erythropalum scandens [J]. Strait Pharm J, 2023, 35(2): 27-30.

引物名称 Primer name	引物序列 Primer sequence F （5′-3′）	引物序列 Primer sequence R （5′-3′）
EsWRI1-1	ATCGGCAGGGGACAATGAG	ATAGAGTCACCCGCACAGGC
EsWRI1-2	AGTAAAATCTGAAGCCAGCCCA	CTCAAACCGTCCAGTCCATCTAT
EsWRI1-4	CAAAGCCGCAAGAACACTACTC	GCCAAACACCCTCCCAATC
EsWRI1-5	CCTCCGTGTCTAATGCCGTT	TGGTAGTACATGCTGTCTAAGCTCA
EsWRI1-6	TGCCGCCAAGAACCCTAA	CCCCACATTCACAAAACCGT
EsWRI1-7	GAGAAGGGGATGGATGTGGA	GCAACCGATGAAGCAGTGG
EsWRI1-8	TCACTATGAAAGCAACGGCAG	TGGGTATTGTGGAACCTGAATCT
EsWRI1-9	AGGATTTTCGGGTTCTCGGT	TGCGAAACCTCCGTAGACTT
EsWRI1-10	CCTACACCCTTCTTCCTGCA	GCATCTCCTCCCTGATCGAA
EsWRI1-11	ACGTCAGAACACCCTCCTTT	GAATGAATGGCAGCAGAGGG
EsWRI1-13	TGGGGTCAGTCATTGCTCAT	TGATCATACCCCGCAACCTT
EsWRI1-14	TTGAGATGAGCCGCTACGAT	AGATGGTGGGAATTGGCTGA
EsWRI1-15	CAACGACGAGGCTTCTGATG	GAAATCCCCTCCTCCACCAA
EsWRI1-16	AAAATGCCACCATCAACCC	TTCCATTGCCACTTCCAACG
EsWRI1-17	TACCCCAATGCCATCACTGT	AAGAAGTGTTGGCGGTTGAC
EsWRI1-ACTIN	CTGGACTCTGGTGATGGTGT	AGCTGTAGTGGTGAACGAGT

引物名称 Primer name	引物序列 Primer sequence F （5′-3′）	引物序列 Primer sequence R （5′-3′）
EsWRI1-1	ATCGGCAGGGGACAATGAG	ATAGAGTCACCCGCACAGGC
EsWRI1-2	AGTAAAATCTGAAGCCAGCCCA	CTCAAACCGTCCAGTCCATCTAT
EsWRI1-4	CAAAGCCGCAAGAACACTACTC	GCCAAACACCCTCCCAATC
EsWRI1-5	CCTCCGTGTCTAATGCCGTT	TGGTAGTACATGCTGTCTAAGCTCA
EsWRI1-6	TGCCGCCAAGAACCCTAA	CCCCACATTCACAAAACCGT
EsWRI1-7	GAGAAGGGGATGGATGTGGA	GCAACCGATGAAGCAGTGG
EsWRI1-8	TCACTATGAAAGCAACGGCAG	TGGGTATTGTGGAACCTGAATCT
EsWRI1-9	AGGATTTTCGGGTTCTCGGT	TGCGAAACCTCCGTAGACTT
EsWRI1-10	CCTACACCCTTCTTCCTGCA	GCATCTCCTCCCTGATCGAA
EsWRI1-11	ACGTCAGAACACCCTCCTTT	GAATGAATGGCAGCAGAGGG
EsWRI1-13	TGGGGTCAGTCATTGCTCAT	TGATCATACCCCGCAACCTT
EsWRI1-14	TTGAGATGAGCCGCTACGAT	AGATGGTGGGAATTGGCTGA
EsWRI1-15	CAACGACGAGGCTTCTGATG	GAAATCCCCTCCTCCACCAA
EsWRI1-16	AAAATGCCACCATCAACCC	TTCCATTGCCACTTCCAACG
EsWRI1-17	TACCCCAATGCCATCACTGT	AAGAAGTGTTGGCGGTTGAC
EsWRI1-ACTIN	CTGGACTCTGGTGATGGTGT	AGCTGTAGTGGTGAACGAGT

基因ID Gene ID	基因名称 Gene name	氨基酸数量 Number of amino acids	分子量 Molecular weight （Da）	理论等电点 Theoretical pI	不稳定指数 Instability index	脂肪族氨基酸指数 Aliphatic index	亲水度 Grand average of hydropathicity	亚细胞定位预测 Prediction of subcellular localizations
rna-Esc18949.1	EsWRI1-1	366	40 146.65	5.63	72.25	61.45	-0.684	细胞核
rna-Esc20888.1	EsWRI1-2	414	46 482.77	8.17	68.63	67.63	-0.652	细胞核
rna-Esc17587.1	EsWRI1-3	395	45 425.88	8.54	56.95	67.19	-0.732	细胞核
rna-Esc03120.1	EsWRI1-4	359	40 429.59	7.25	52.93	53.93	-0.845	叶绿体
rna-Esc06811.1	EsWRI1-5	654	72 603.55	6.60	49.21	58.65	-0.705	细胞核
rna-Esc08324.1	EsWRI1-6	505	55 072.66	6.68	43.03	61.31	-0.590	细胞核
rna-Esc21664.1	EsWRI1-7	455	49 570.36	6.10	49.52	68.44	-0.428	细胞核
rna-Esc10505.1	EsWRI1-8	682	75 623.87	6.44	64.94	56.00	-0.727	细胞核
rna-Esc10658.1	EsWRI1-9	516	56 494.17	6.26	52.68	51.65	-0.784	细胞核
rna-Esc09593.1	EsWRI1-10	373	41 400.93	6.56	69.97	54.21	-0.760	叶绿体
rna-Esc11447.1	EsWRI1-11	498	54 081.18	6.11	58.43	61.75	-0.541	细胞核
rna-Esc07556.1	EsWRI1-12	776	86 018.87	7.65	38.19	64.34	-0.558	细胞核
rna-Esc20152.1	EsWRI1-13	626	68 403.11	5.96	43.21	57.86	-0.632	细胞外基质
rna-Esc10394.1	EsWRI1-14	495	54 505.45	5.82	46.52	66.10	-0.464	细胞核
rna-Esc02568.1	EsWRI1-15	451	49 572.57	5.06	50.92	64.32	-0.610	细胞核
rna-Esc07558.1	EsWRI1-16	606	66 890.17	7.71	49.21	59.75	-0.734	细胞核
rna-Esc09123.1	EsWRI1-17	469	51 678.94	8.93	48.29	61.81	-0.575	细胞核

基因ID Gene ID	基因名称 Gene name	氨基酸数量 Number of amino acids	分子量 Molecular weight （Da）	理论等电点 Theoretical pI	不稳定指数 Instability index	脂肪族氨基酸指数 Aliphatic index	亲水度 Grand average of hydropathicity	亚细胞定位预测 Prediction of subcellular localizations
rna-Esc18949.1	EsWRI1-1	366	40 146.65	5.63	72.25	61.45	-0.684	细胞核
rna-Esc20888.1	EsWRI1-2	414	46 482.77	8.17	68.63	67.63	-0.652	细胞核
rna-Esc17587.1	EsWRI1-3	395	45 425.88	8.54	56.95	67.19	-0.732	细胞核
rna-Esc03120.1	EsWRI1-4	359	40 429.59	7.25	52.93	53.93	-0.845	叶绿体
rna-Esc06811.1	EsWRI1-5	654	72 603.55	6.60	49.21	58.65	-0.705	细胞核
rna-Esc08324.1	EsWRI1-6	505	55 072.66	6.68	43.03	61.31	-0.590	细胞核
rna-Esc21664.1	EsWRI1-7	455	49 570.36	6.10	49.52	68.44	-0.428	细胞核
rna-Esc10505.1	EsWRI1-8	682	75 623.87	6.44	64.94	56.00	-0.727	细胞核
rna-Esc10658.1	EsWRI1-9	516	56 494.17	6.26	52.68	51.65	-0.784	细胞核
rna-Esc09593.1	EsWRI1-10	373	41 400.93	6.56	69.97	54.21	-0.760	叶绿体
rna-Esc11447.1	EsWRI1-11	498	54 081.18	6.11	58.43	61.75	-0.541	细胞核
rna-Esc07556.1	EsWRI1-12	776	86 018.87	7.65	38.19	64.34	-0.558	细胞核
rna-Esc20152.1	EsWRI1-13	626	68 403.11	5.96	43.21	57.86	-0.632	细胞外基质
rna-Esc10394.1	EsWRI1-14	495	54 505.45	5.82	46.52	66.10	-0.464	细胞核
rna-Esc02568.1	EsWRI1-15	451	49 572.57	5.06	50.92	64.32	-0.610	细胞核
rna-Esc07558.1	EsWRI1-16	606	66 890.17	7.71	49.21	59.75	-0.734	细胞核
rna-Esc09123.1	EsWRI1-17	469	51 678.94	8.93	48.29	61.81	-0.575	细胞核