大白菜LEA家族基因的鉴定及其部分成员在低温胁迫下的表达分析

doi:10.16420/j.issn.0513-353x.2021-0044

摘要/Abstract

摘要：

基于大白菜全基因组数据对LEA家族基因进行全基因组鉴定与生物信息学分析,研究其序列特征、基因结构、启动子顺式作用元件、染色体定位、进化关系以及在不同组织中和低温胁迫下的表达模式。从大白菜基因组中总共鉴定出65个LEA家族基因成员,根据系统发育与保守基序分析,其可分为8个组;内含子较少,且不均匀地分布在10条染色体上,另有3个成员位于Scaffold上。启动子顺式作用元件分析显示,有29个（44.6%）成员拥有低温响应元件,除此之外,光响应元件和激素响应元件占比较高。共线性分析显示,大白菜BrLEA与拟南芥AtLEA同源性较高,并在进化中较为保守。大白菜不同组织转录组数据表明,BrLEA基因在大白菜不同组织中的表达存在组织特异性。对筛选出的13个家族成员进行低温胁迫表达分析表明,受低温胁迫表达量都有所升高。

关键词: 大白菜, LEA基因家族, 低温胁迫, 生物信息学

Abstract:

This study was based on the whole genome data of Chinese cabbage to identify and bioinformatics the late embryogenesis abundant protein（LEA）family genes. The sequence characteristics,gene structure,promoter cis-acting elements,chromosome localization,evolutionary relationships,and expression patterns in different tissues and under low temperature stress were investigated. The results showed that 65 family members were identified from the Chinese cabbage genome and could be divided into eight groups according to phylogenetic and conserved motif analysis. Fewer introns are prevalent and unevenly distributed on ten chromosomes,with three other members located on the Scaffold. The promoter cis-acting element analysis showed that 29 members（44.6%）had low temperature response elements. In addition,the proportion of light response elements and hormone response elements was the highest. The collinearity analysis showed that BrLEAs and AtLEAs had higher homology and were conservative in evolution. Analysis of transcriptome data of different tissues of Chinese cabbage found that the expression of BrLEA genes in different tissues was different and had tissue specificity. The expression of 13 family members under low temperature stress family members showed that the expression of low temperature stress increased.

Key words: Chinese cabbage, gene family of LEA, low temperature stress, bioinformatics

中图分类号:

S634.1

王光鹏, 刘同坤, 徐新凤, 李竹帛, 高瞻远, 侯喜林. 大白菜LEA家族基因的鉴定及其部分成员在低温胁迫下的表达分析[J]. 园艺学报, 2022, 49(2): 304-318.

WANG Guangpeng, LIU Tongkun, XU Xinfeng, LI Zhubo, GAO Zhanyuan, HOU Xilin. Identification of LEA Family and Expression Analysis of Some Members Under Low-temperature Stress in Chinese Cabbage[J]. Acta Horticulturae Sinica, 2022, 49(2): 304-318.

图/表 8

参考文献 42

[1]	Amara I, Odena A, Oliveira E, Moreno A, Masmoudi K, Pagès M, Goday A. 2012. Insights into maize LEA proteins:from proteomics to functional approaches. Plant Cell Physiol, 53 (2):312-329. doi: 10.1093/pcp/pcr183 pmid: 22199372
[2]	Baker J, Van Dennsteele C, Dure L. 1988. Sequence and characterization of 6 LEA proteins and their genes from cotton. Plant Mol Biol, 11 (3):277-291. doi: 10.1007/BF00027385 pmid: 24272341
[3]	Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias A A. 2008. The enigmatic LEA proteins and other hydrophilins. Plant Physiol, 148 (1):6-24. doi: 10.1104/pp.108.120725 pmid: 18772351
[4]	Bies-Ethève N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, Raynal M, Cooke R, Delseny M. 2008. Inventory,evolution and expression profiling diversity of the LEA(late embryogenesis abundant)protein gene family in Arabidopsis thaliana. Plant Mol Biol, 67 (1-2):107-124. doi: 10.1007/s11103-008-9304-x pmid: 18265943
[5]	Candat A, Paszkiewicz G, Neveu M, Gautier R, Logan D C, Avelange-Macherel M H, Macherel D. 2014. The ubiquitous distribution of late embryogenesis abundant proteins across cell compartments in Arabidopsis offers tailored protection against abiotic stress. Plant Cell, 26 (7):3148-3166. doi: 10.1105/tpc.114.127316 URL
[6]	Cao J, Li X. 2015. Identification and phylogenetic analysis of late embryogenesis abundant proteins family in tomato(Solanum lycopersicum). Planta, 241 (3):757-772. doi: 10.1007/s00425-014-2215-y URL
[7]	Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. 2020. TBtools:an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 13 (8):1194-1202. doi: 10.1016/j.molp.2020.06.009 URL
[8]	Chen Fang, Gu Xiaoping, Liang Ping, Yu Fei. 2017. Effects of low temperature freezing injury on morphological changes of Chinese cabbage. Meteorological and Environmental Sciences, 40 (2):55-59. (in Chinese)
	陈芳, 谷晓平, 梁平, 于飞. 2017. 低温冻害对大白菜形态变化的影响. 气象与环境科学, 40 (2):55-59.
[9]	Chen Yiyin. 2007. Study on cold resistance of tobacco and transgenic plants induced by low temperature gene transformation of Amongillus amurensis[M. D. Dissertation]. BeiJing: Beijing Forestry University. (in Chinese)
	陈奕吟. 2007. 沙冬青低温诱导基因转化烟草及转基因植物的抗寒性研究[硕士论文]. 北京: 北京林业大学.
[10]	Daniel C J, Christopher J P, Jürg B. 2008. Rapidly regulated genes are intron poor. Trends Genet, 24 (8):375-378. doi: 10.1016/j.tig.2008.05.006 URL
[11]	Du Yongting, Wang Tiejuan, Du Junrui, Chen Jing. 2018. Expression and sequence analysis of LEA gene of Artemisia argyi under drought stress. Biotechnology, 28 (4):318-322,371. (in Chinese)
	杜永婷, 王铁娟, 杜俊瑞, 陈静. 2018. 干旱胁迫下白沙蒿LEA基因的表达及序列分析. 生物技术, 28 (4):318-322,371.
[12]	Dure L Ⅲ. 1993. A repeating 11-mer amino acid motif and plant desiccation. Plant J, 3 (3):363-369. pmid: 8220448
[13]	Dure L Ⅲ, Crouch M, Harada J, Ho T H, Mundy J, Quatrano R, Thomas T, Sung Z R. 1989. Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol, 12 (5):475-486. doi: 10.1007/BF00036962 pmid: 24271064
[14]	Dure L Ⅲ, Greenway S C, Galau G A. 1981. Developmental biochemistry of cottonseed embryogenesis and germination:changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry, 20 (14):4162-4168. pmid: 7284317
[15]	Espelund M, Saebøe-Larssen S, Hughes D W, Galau G A, Larsen F, Jakobsen K S. 1992. Late embryogenesis-abundant genes encoding proteins with different numbers of hydrophilic repeats are regulated differentially by abscisic acid and osmotic stress. Plant J, 2 (2):241-252. pmid: 1302052
[16]	Finn R D, Mistry J, Tate J, Coggill P, Heger A, Pollington J E, Gavin O L, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer E L, Eddy R, Bateman A. 2000. The Pfam protein families database. Nucleic Acids Res, 38 (Database issue):D211-D222.
[17]	Gao T, Mo Y X, Huang H Y, Yu J M, Wang Y, Wang W D. 2021. Heterologous expression of Camellia sinensis late embryogenesis abundant protein gene 1(CsLEA1)confers cold stress tolerance in Escherichia coli and yeast. Horticultural Plant Journal, 7 (1):89-96. doi: 10.1016/j.hpj.2020.09.005 URL
[18]	Garay-Arroyo A, Colmener-Flores J M, Garciarrubio A, Covarrubias A A. 2000. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J Biol Chem, 275 (8):5668-5674. doi: 10.1074/jbc.275.8.5668 pmid: 10681550
[19]	Hand S C, Menze M A, Toner M, Boswell L, Moore D. 1996. LEA proteins during water stress:not just for plants anymore. Annu Rev Physiol, 73:115-134. doi: 10.1146/physiol.2011.73.issue-1 URL
[20]	Hundertmark M, Hincha D K. 2008. LEA(late embryogenesis abundant)proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics, 9 (1):118. doi: 10.1186/1471-2164-9-118 URL
[21]	Imai R, Chang L, Ohta A, Bray E A, Takagi M. 1996. A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisiae. Gene, 170 (2):243-248. pmid: 8666253
[22]	Jeffares D C, Penkett C J, Bähler J. 2008. Rapidly regulated genes are intron poor. Trends Genet, 24 (8):375-378. doi: 10.1016/j.tig.2008.05.006 pmid: 18586348
[23]	Kosová K, Vítámvás Prášil, Prasil I. 2007. The role of dehydrins in plant response to cold. Biol Plant, 51 (4):601-617. doi: 10.1007/s10535-007-0133-6 URL
[24]	Lysak M A, Koch M A, Pecinka A, Schubert I. 2005. Chromosome triplication found across the tribe Brassiceae. Genome Res, 15 (4):516-525. doi: 10.1101/gr.3531105 URL
[25]	Liu Y, Xie L, Liang X, Zhang S. 2015. pLEA5,the Late Embryogenesis Abundant Protein Gene from Chimonanthus praecox,possesses low temperature and osmotic resistances in prokaryote and eukaryotes. Int J Mol Sci, 16 (11):26978-26990. doi: 10.3390/ijms161126006 URL
[26]	Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Langridge P, Lopato S. 2011. Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J, 9 (2):230-249. doi: 10.1111/j.1467-7652.2010.00547.x pmid: 20642740
[27]	Mowla S B, Cuypers A, Driscoll S P, Kiddle G, Thomson J, Foyer C H, Theodoulou F L. 2006. Yeast complementation reveals a role for an Arabidopsis thaliana late embryogenesis abundant(LEA)-like protein in oxidative stress tolerance. Plant J, 48 (5):743-756. doi: 10.1111/tpj.2006.48.issue-5 URL
[28]	Nagaraju M, Kumar S A, Reddy P S, Kumar A, Rao D M, Kavi Kishor P B. 2019. Genome-scale identification,classification,and tissue specific expression analysis of late embryogenesis abundant(LEA)genes under abiotic stress conditions in Sorghum bicolor L. PLoS ONE, 14 (1):e0209980. doi: 10.1371/journal.pone.0209980 URL
[29]	Olvera-Carrillo Y, Luis Reyes J, Covarrubias A A. 2011. Late embryogenesis abundant proteins:versatile players in the plant adaptation to water limiting environments. Plant Signal Behav, 6 (4):586-589. doi: 10.4161/psb.6.4.15042 pmid: 21447997
[30]	Park S C, Kim Y H, Jeong J C, Kim C Y, Lee H S, Bang J W, Kwak S S. 2011. Sweetpotato late embryogenesis abundant 14(IbLEA14)gene influences lignification and increases osmotic- and salt stress-tolerance of transgenic calli. Planta, 233 (3):621-634. doi: 10.1007/s00425-010-1326-3 URL
[31]	Tong C, Wang X, Yu J, Wu J, Li W, Huang J, Dong C, Hua W, Liu S. 2013. Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa. BMC Genomics, 14:689. doi: 10.1186/1471-2164-14-689 URL
[32]	Tunnacliffe A, Wise M J. 2007. The continuing conundrum of the LEA proteins. Naturwissenschaften, 94 (10):791-812. doi: 10.1007/s00114-007-0254-y URL
[33]	Wang Ying, Zhang Changwei, Lv Shanwu, Hou Xilin. 2018. Genome identification and expression analysis BrCNGC Chinese cabbage. Journal of Nanjing Agricultural University, 41 (6):994-1002. (in Chinese)
	汪影, 张昌伟, 吕善武, 侯喜林. 2018. 大白菜BrCNGC全基因组鉴定及其表达分析. 南京农业大学学报, 41 (6):994-1002.
[34]	Wang X S, Zhu H B, Jin G L, Liu H L, Wu W R, Zhu J. 2006. Genome-scale identification and analysis of LEA genes in rice ( Oryza sativa L.). Plant Science, 172 (2):414-420. doi: 10.1016/j.plantsci.2006.10.004 URL
[35]	Wang Y D, Chen G J, Lei J J, Cao B H, Chen C M. 2020. Identification and characterization of a LEA-like gene,CaMF5,specifically expressed in the anthers of male-fertile Capsicum annuum. Horticultural Plant Journal, 6 (1):39-48. doi: 10.1016/j.hpj.2019.07.004 URL
[36]	Wise M J, Tunnacliffe A. 2004. POPP the question:what do LEA proteins do? Trends Plant Sci, 9 (1):13-17. doi: 10.1016/j.tplants.2003.10.012 URL
[37]	Yu J, Lai Y, Wu X, Wu G, Guo C. 2016. Overexpression of OsEm1 encoding a group I LEA protein confers enhanced drought tolerance in rice. Biochem Biophys Res Commun, 478 (2):703-709. doi: 10.1016/j.bbrc.2016.08.010 URL
[38]	Yu J N, Zhang J S, Shan L, Chen S Y. 2005. Two new group 3 LEA genes of wheat and their functional analysis in yeast. Journal of Integrative Plant Biology Formerly Aacta Botanica Sinica, 47 (11):1372-1381.
[39]	Zhang L, Cai X, Wu J, Liu M, Grob S, Cheng F, Liang J, Cai C, Liu Z, Liu B, Wang F, Li S, Li X, Cheng L, Yang W, Li M H, Grossniklaus U, Zheng H, Wang X. 2019. Improved Brassica rapa reference genome by single-molecule sequencing and chromosome conformation capture technologies. Hortic Res, 13 (6):124.
[40]	Zhang L S, Zhao W M. 2003. LEA protein functions to tolerance drought of the plant. Plant Physiol Comm, 39:61-66.
[41]	Zhang Mei, Zhang Hui. 2017. Research progress in late embryogenesis abundant protein(LEA protein)and plant stress resistance. Biotic Resources, 39 (3):155-161. (in Chinese)
	张美, 张会. 2017. 胚胎发育晚期丰富蛋白(LEA蛋白)与植物抗逆性研究进展. 生物资源, 39 (3):155-161.
[42]	Zong Mei, Cai Yongping. 2005. Correlation between seed dehydration tolerance and protective system. Acta Horticulturae Sinica, 46 (2):342-347. (in Chinese)
	宗梅, 蔡永萍. 2005. 种子脱水耐性与保护系统的相关性. 园艺学报, 46 (2):342-347.

基因 ID Gene ID	基因名称 Gene name	引物序列（5′-3′） Primer sequence
Bra008242	BrDehydrin2	F：GGAATCATCAGCGGAGGTCA;R：CCTCGTGTTTAACCTCAGGCA
Bra025819	BrDehydrin4	F：TTCCGGTGAAGGAGGAAACG;R：CCGTGTCGACCACTTGAGAA
Bra012230	BrDehydrin5	F：TTCACCGATCCAACAGCTCC;R：CCTCCGTGTTGACGACTTGA
Bra015779	BrDehydrin6	F：AGGAATCATCAACGGCCACC;R：CACCGGCTCTGAGATGTGAA
Bra003732	BrDehydrin7	F：AGGACACGGAAAGAAACCCG;R：CCTCAACGGTCTTTGAGTGG
Bra013992	BrDehydrin8	F：TGCAGCTTCCAAAGGTTGTG;R：CGTCGCGTCAGTCACATAGA
Bra035491	BrLEA_1-3	F：GGGCACGGACTAAAGAGGAG;R：TCACAGGTGTGTGATGAGGC
Bra000414	BrLEA_2-2	F：AAGGACGATAGCGTCGGGTA;R：CCGCTATGCTATAGGCCACC
Bra026541	BrLEA_4-3	F：GAATGCGACCATTACACCGC;R：CCACTTCACTCCCCATGTCC
Bra000263	BrLEA_4-6	F：GGCCTTGAAAAATGGCGAGA;R：TTTGTGGCGTCCTTAGCCTC
Bra000265	BrLEA_4-7	F：CTCAGGAGCTGTTCTCAGTGG;R：ATCAACGACTTCTTGCGCTG
Bra000173	BrLEA_5-1	F：GCCGAGGAGGGAATACAAGG;R：TGGGTTCGTCCATCTCCTCT
Bra022950	BrLEA_6-1	F：GCCACTAGAAACGAGTCCGTA;R：GGCCATGCTTAACCTGTTGG
	Actin	F：AGGCTACACGTTCGGACAAG;R：TGGGGCACTAAACACAGTCA

基因 ID Gene ID	基因名称 Gene name	引物序列（5′-3′） Primer sequence
Bra008242	BrDehydrin2	F：GGAATCATCAGCGGAGGTCA;R：CCTCGTGTTTAACCTCAGGCA
Bra025819	BrDehydrin4	F：TTCCGGTGAAGGAGGAAACG;R：CCGTGTCGACCACTTGAGAA
Bra012230	BrDehydrin5	F：TTCACCGATCCAACAGCTCC;R：CCTCCGTGTTGACGACTTGA
Bra015779	BrDehydrin6	F：AGGAATCATCAACGGCCACC;R：CACCGGCTCTGAGATGTGAA
Bra003732	BrDehydrin7	F：AGGACACGGAAAGAAACCCG;R：CCTCAACGGTCTTTGAGTGG
Bra013992	BrDehydrin8	F：TGCAGCTTCCAAAGGTTGTG;R：CGTCGCGTCAGTCACATAGA
Bra035491	BrLEA_1-3	F：GGGCACGGACTAAAGAGGAG;R：TCACAGGTGTGTGATGAGGC
Bra000414	BrLEA_2-2	F：AAGGACGATAGCGTCGGGTA;R：CCGCTATGCTATAGGCCACC
Bra026541	BrLEA_4-3	F：GAATGCGACCATTACACCGC;R：CCACTTCACTCCCCATGTCC
Bra000263	BrLEA_4-6	F：GGCCTTGAAAAATGGCGAGA;R：TTTGTGGCGTCCTTAGCCTC
Bra000265	BrLEA_4-7	F：CTCAGGAGCTGTTCTCAGTGG;R：ATCAACGACTTCTTGCGCTG
Bra000173	BrLEA_5-1	F：GCCGAGGAGGGAATACAAGG;R：TGGGTTCGTCCATCTCCTCT
Bra022950	BrLEA_6-1	F：GCCACTAGAAACGAGTCCGTA;R：GGCCATGCTTAACCTGTTGG
	Actin	F：AGGCTACACGTTCGGACAAG;R：TGGGGCACTAAACACAGTCA

基因号 Gene number	基因名称 Gene name	氨基酸长度 Amino acid length	等电点 pI	分子量/D MW	不稳定性指数 Instability index	脂肪族指数 Aliphatic index	亲水性 GRAVY	亚细胞定位 Subcellular localization
Bra011874	BrDehydrin-1	149	5.65	15 928.40	23.71	58.93	-0.863	细胞核 Nucleus
Bra036843	BrDehydrin-10	134	9.19	13 834.22	42.98	49.55	-0.887	细胞核 Nucleus
Bra037177	BrDehydrin-11	144	8.81	15 139.46	45.61	33.26	-1.360	细胞核 Nucleus
Bra008242	BrDehydrin-2	194	5.52	21 840.38	62.43	53.71	-1.352	细胞核 Nucleus
Bra031809	BrDehydrin-3	192	7.14	18 844.17	33.09	32.14	-1.021	细胞核 Nucleus
Bra025819	BrDehydrin-4	271	5.00	31 018.16	61.44	47.49	-1.508	细胞核 Nucleus
Bra012230	BrDehydrin-5	220	5.11	24 837.39	62.24	55.41	-1.399	细胞核 Nucleus
Bra015779	BrDehydrin-6	195	5.45	22 044.52	63.15	50.41	-1.455	细胞核 Nucleus
Bra003732	BrDehydrin-7	194	5.47	21 755.35	56.38	53.25	-1.308	细胞核 Nucleus
Bra013992	BrDehydrin-8	257	6.17	28 978.00	34.53	35.33	-1.645	细胞核 Nucleus
Bra031192	BrDehydrin-9	183	6.49	19 183.88	36.64	49.18	-1.016	细胞核 Nucleus
Bra005911	BrLEA_1-1	159	9.22	16 286.99	17.53	43.71	-0.789	细胞核 Nucleus
Bra005353	BrLEA_1-2	98	9.22	10 666.89	42.18	49.18	-1.115	细胞核 Nucleus
Bra035491	BrLEA_1-3	132	9.68	14 933.95	56.61	51.89	-1.109	线粒体 Mitochondrion
Bra023278	BrLEA_1-4	133	9.24	14 507.53	59.47	48.65	-0.878	线粒体 Mitochondrion
Bra009225	BrLEA_1-5	159	8.93	16 180.83	16.45	38.81	-0.818	细胞核 Nucleus
Bra000339	BrLEA_2-1	777	9.02	84 314.53	32.33	96.22	-0.135	叶绿体 Chloroplast
Bra000414	BrLEA_2-2	166	4.81	17 823.38	17.04	96.81	0.030	胞外Extracellular
Bra039288	BrLEA_2-3	166	4.50	18 119.88	16.96	100.36	0.013	叶绿体 Chloroplast
Bra037669	BrLEA_2-4	506	8.85	55 465.06	27.06	85.89	-0.399	细胞核 Nucleus
Bra004565	BrLEA_2-5	166	4.81	17 725.34	20.39	106.20	0.093	细胞膜 Cell membrane
Bra030494	BrLEA_2-6	151	4.72	16 404.92	10.57	106.42	0.075	细胞膜 Cell membrane
Bra033520	BrLEA_3-1	99	9.72	10 582.01	50.01	70.10	-0.400	叶绿体 Chloroplast
Bra000884	BrLEA_3-2	94	9.85	10 095.53	39.42	78.94	-0.349	叶绿体 Chloroplast
Bra014864	BrLEA_3-3	122	9.20	14 152.16	50.98	63.20	-0.598	叶绿体 Chloroplast
Bra018556	BrLEA_3-4	93	9.99	10 112.56	52.38	72.47	-0.482	叶绿体 Chloroplast
Bra038061	BrLEA_3-5	57	4.94	6 614.40	49.22	56.67	-0.912	线粒体 Mitochondrion
Bra036272	BrLEA_3-6	94	9.99	10 088.55	43.90	72.77	-0.299	叶绿体 Chloroplast
Bra033350	BrLEA_3-7	98	8.03	10 298.59	40.91	76.84	-0.229	叶绿体 Chloroplast
Bra021126	BrLEA_4-1	226	9.02	24 598.55	28.79	22.79	-1.475	线粒体 Mitochondrion
Bra022221	BrLEA_4-10	298	5.45	32 431.59	30.10	54.50	-1.126	胞外Extracellular
Bra027219	BrLEA_4-11	229	8.83	24 810.86	27.04	22.97	-1.414	线粒体 Mitochondrion
Bra005256	BrLEA_4-12	399	5.74	43 565.34	20.90	52.93	-0.970	细胞膜 Cell membrane
Bra019628	BrLEA_4-13	451	5.20	48 554.47	12.26	47.98	-1.141	细胞核 Nucleus
Bra025130	BrLEA_4-14	201	5.40	22 054.03	38.33	77.21	-0.429	叶绿体 Chloroplast
Bra039616	BrLEA_4-15	480	6.47	52 652.67	18.82	47.04	-0.921	叶绿体 Chloroplast
Bra010561	BrLEA_4-16	487	5.63	52 431.94	23.72	46.65	-0.923	叶绿体 Chloroplast
Bra020879	BrLEA_4-17	218	5.12	24 376.73	15.32	38.72	-1.441	细胞核 Nucleus
Bra027542	BrLEA_4-18	311	7.60	35 005.70	23.66	43.79	-1.371	叶绿体 Chloroplast
Bra037225	BrLEA_4-19	722	8.58	80 928.05	43.18	68.66	-0.722	叶绿体 Chloroplast
Bra013489	BrLEA_4-2	253	8.55	27 837.93	20.67	47.31	-1.202	叶绿体 Chloroplast
Bra036021	BrLEA_4-20	253	5.72	28 430.30	32.23	43.72	-1.355	叶绿体 Chloroplast
Bra041061	BrLEA_4-21	241	6.17	26 330.13	20.46	50.83	-1.111	叶绿体 Chloroplast
Bra026541	BrLEA_4-3	192	8.57	20 399.00	33.96	62.55	-0.669	叶绿体 Chloroplast
Bra008006	BrLEA_4-4	462	9.03	50 701.68	32.68	78.53	-0.390	胞外Extracellular
Bra001666	BrLEA_4-5	276	5.54	30 311.37	25.62	53.22	-1.093	叶绿体 Chloroplast
Bra000263	BrLEA_4-6	142	8.65	14 760.62	19.57	77.75	-0.430	叶绿体 Chloroplast
Bra000265	BrLEA_4-7	129	5.31	13 894.51	22.81	71.86	-0.692	叶绿体 Chloroplast
Bra017229	BrLEA_4-8	398	6.02	43 386.25	20.77	55.63	-1.065	细胞核 Nucleus
Bra016868	BrLEA_4-9	679	5.98	72 972.61	33.88	45.77	-1.088	细胞核 Nucleus
Bra000173	BrLEA_5-1	88	5.88	9 630.38	37.14	25.57	-1.659	线粒体 Mitochondrion
Bra004981	BrLEA_5-2	84	6.74	9 264.98	49.89	27.96	-1.704	线粒体 Mitochondrion
Bra040894	BrLEA_5-3	172	6.17	18 997.70	42.85	30.64	-1.635	细胞核 Nucleus
Bra022950	BrLEA_6-1	71	6.03	7 581.23	52.98	40.00	-1.238	细胞核 Nucleus
Bra021869	BrLEA_6-2	72	5.21	7 627.30	58.73	40.83	-1.174	细胞核 Nucleus
Bra039946	BrLEA_6-3	82	4.72	8 433.11	44.84	37.07	-1.055	线粒体 Mitochondrion
Bra022642	BrSMP-1	173	5.88	18 379.46	40.43	86.36	-0.357	细胞膜 Cell membrane
Bra020604	BrSMP-2	181	4.76	18 366.26	31.03	71.44	-0.481	细胞核 Nucleus
Bra001869	BrSMP-3	239	5.70	25 385.45	46.14	76.78	-0.380	细胞膜 Cell membrane
Bra029085	BrSMP-4	177	5.43	18 691.81	41.22	82.20	-0.351	细胞膜 Cell membrane
Bra039956	BrSMP-5	262	4.71	26 692.50	34.19	77.21	-0.239	细胞膜 Cell membrane
Bra009983	BrSMP-6	192	4.76	19 473.41	23.22	69.32	-0.515	细胞膜 Cell membrane
Bra036112	BrSMP-7	191	4.99	19 600.77	26.99	75.81	-0.414	细胞核 Nucleus
Bra033375	BrSMP-8	177	4.53	18 185.98	30.21	71.24	-0.540	叶绿体 Chloroplast
Bra033377	BrSMP-9	283	8.89	32 586.25	52.20	75.72	-0.543	叶绿体 Chloroplast

基因号 Gene number	基因名称 Gene name	氨基酸长度 Amino acid length	等电点 pI	分子量/D MW	不稳定性指数 Instability index	脂肪族指数 Aliphatic index	亲水性 GRAVY	亚细胞定位 Subcellular localization
Bra011874	BrDehydrin-1	149	5.65	15 928.40	23.71	58.93	-0.863	细胞核 Nucleus
Bra036843	BrDehydrin-10	134	9.19	13 834.22	42.98	49.55	-0.887	细胞核 Nucleus
Bra037177	BrDehydrin-11	144	8.81	15 139.46	45.61	33.26	-1.360	细胞核 Nucleus
Bra008242	BrDehydrin-2	194	5.52	21 840.38	62.43	53.71	-1.352	细胞核 Nucleus
Bra031809	BrDehydrin-3	192	7.14	18 844.17	33.09	32.14	-1.021	细胞核 Nucleus
Bra025819	BrDehydrin-4	271	5.00	31 018.16	61.44	47.49	-1.508	细胞核 Nucleus
Bra012230	BrDehydrin-5	220	5.11	24 837.39	62.24	55.41	-1.399	细胞核 Nucleus
Bra015779	BrDehydrin-6	195	5.45	22 044.52	63.15	50.41	-1.455	细胞核 Nucleus
Bra003732	BrDehydrin-7	194	5.47	21 755.35	56.38	53.25	-1.308	细胞核 Nucleus
Bra013992	BrDehydrin-8	257	6.17	28 978.00	34.53	35.33	-1.645	细胞核 Nucleus
Bra031192	BrDehydrin-9	183	6.49	19 183.88	36.64	49.18	-1.016	细胞核 Nucleus
Bra005911	BrLEA_1-1	159	9.22	16 286.99	17.53	43.71	-0.789	细胞核 Nucleus
Bra005353	BrLEA_1-2	98	9.22	10 666.89	42.18	49.18	-1.115	细胞核 Nucleus
Bra035491	BrLEA_1-3	132	9.68	14 933.95	56.61	51.89	-1.109	线粒体 Mitochondrion
Bra023278	BrLEA_1-4	133	9.24	14 507.53	59.47	48.65	-0.878	线粒体 Mitochondrion
Bra009225	BrLEA_1-5	159	8.93	16 180.83	16.45	38.81	-0.818	细胞核 Nucleus
Bra000339	BrLEA_2-1	777	9.02	84 314.53	32.33	96.22	-0.135	叶绿体 Chloroplast
Bra000414	BrLEA_2-2	166	4.81	17 823.38	17.04	96.81	0.030	胞外Extracellular
Bra039288	BrLEA_2-3	166	4.50	18 119.88	16.96	100.36	0.013	叶绿体 Chloroplast
Bra037669	BrLEA_2-4	506	8.85	55 465.06	27.06	85.89	-0.399	细胞核 Nucleus
Bra004565	BrLEA_2-5	166	4.81	17 725.34	20.39	106.20	0.093	细胞膜 Cell membrane
Bra030494	BrLEA_2-6	151	4.72	16 404.92	10.57	106.42	0.075	细胞膜 Cell membrane
Bra033520	BrLEA_3-1	99	9.72	10 582.01	50.01	70.10	-0.400	叶绿体 Chloroplast
Bra000884	BrLEA_3-2	94	9.85	10 095.53	39.42	78.94	-0.349	叶绿体 Chloroplast
Bra014864	BrLEA_3-3	122	9.20	14 152.16	50.98	63.20	-0.598	叶绿体 Chloroplast
Bra018556	BrLEA_3-4	93	9.99	10 112.56	52.38	72.47	-0.482	叶绿体 Chloroplast
Bra038061	BrLEA_3-5	57	4.94	6 614.40	49.22	56.67	-0.912	线粒体 Mitochondrion
Bra036272	BrLEA_3-6	94	9.99	10 088.55	43.90	72.77	-0.299	叶绿体 Chloroplast
Bra033350	BrLEA_3-7	98	8.03	10 298.59	40.91	76.84	-0.229	叶绿体 Chloroplast
Bra021126	BrLEA_4-1	226	9.02	24 598.55	28.79	22.79	-1.475	线粒体 Mitochondrion
Bra022221	BrLEA_4-10	298	5.45	32 431.59	30.10	54.50	-1.126	胞外Extracellular
Bra027219	BrLEA_4-11	229	8.83	24 810.86	27.04	22.97	-1.414	线粒体 Mitochondrion
Bra005256	BrLEA_4-12	399	5.74	43 565.34	20.90	52.93	-0.970	细胞膜 Cell membrane
Bra019628	BrLEA_4-13	451	5.20	48 554.47	12.26	47.98	-1.141	细胞核 Nucleus
Bra025130	BrLEA_4-14	201	5.40	22 054.03	38.33	77.21	-0.429	叶绿体 Chloroplast
Bra039616	BrLEA_4-15	480	6.47	52 652.67	18.82	47.04	-0.921	叶绿体 Chloroplast
Bra010561	BrLEA_4-16	487	5.63	52 431.94	23.72	46.65	-0.923	叶绿体 Chloroplast
Bra020879	BrLEA_4-17	218	5.12	24 376.73	15.32	38.72	-1.441	细胞核 Nucleus
Bra027542	BrLEA_4-18	311	7.60	35 005.70	23.66	43.79	-1.371	叶绿体 Chloroplast
Bra037225	BrLEA_4-19	722	8.58	80 928.05	43.18	68.66	-0.722	叶绿体 Chloroplast
Bra013489	BrLEA_4-2	253	8.55	27 837.93	20.67	47.31	-1.202	叶绿体 Chloroplast
Bra036021	BrLEA_4-20	253	5.72	28 430.30	32.23	43.72	-1.355	叶绿体 Chloroplast
Bra041061	BrLEA_4-21	241	6.17	26 330.13	20.46	50.83	-1.111	叶绿体 Chloroplast
Bra026541	BrLEA_4-3	192	8.57	20 399.00	33.96	62.55	-0.669	叶绿体 Chloroplast
Bra008006	BrLEA_4-4	462	9.03	50 701.68	32.68	78.53	-0.390	胞外Extracellular
Bra001666	BrLEA_4-5	276	5.54	30 311.37	25.62	53.22	-1.093	叶绿体 Chloroplast
Bra000263	BrLEA_4-6	142	8.65	14 760.62	19.57	77.75	-0.430	叶绿体 Chloroplast
Bra000265	BrLEA_4-7	129	5.31	13 894.51	22.81	71.86	-0.692	叶绿体 Chloroplast
Bra017229	BrLEA_4-8	398	6.02	43 386.25	20.77	55.63	-1.065	细胞核 Nucleus
Bra016868	BrLEA_4-9	679	5.98	72 972.61	33.88	45.77	-1.088	细胞核 Nucleus
Bra000173	BrLEA_5-1	88	5.88	9 630.38	37.14	25.57	-1.659	线粒体 Mitochondrion
Bra004981	BrLEA_5-2	84	6.74	9 264.98	49.89	27.96	-1.704	线粒体 Mitochondrion
Bra040894	BrLEA_5-3	172	6.17	18 997.70	42.85	30.64	-1.635	细胞核 Nucleus
Bra022950	BrLEA_6-1	71	6.03	7 581.23	52.98	40.00	-1.238	细胞核 Nucleus
Bra021869	BrLEA_6-2	72	5.21	7 627.30	58.73	40.83	-1.174	细胞核 Nucleus
Bra039946	BrLEA_6-3	82	4.72	8 433.11	44.84	37.07	-1.055	线粒体 Mitochondrion
Bra022642	BrSMP-1	173	5.88	18 379.46	40.43	86.36	-0.357	细胞膜 Cell membrane
Bra020604	BrSMP-2	181	4.76	18 366.26	31.03	71.44	-0.481	细胞核 Nucleus
Bra001869	BrSMP-3	239	5.70	25 385.45	46.14	76.78	-0.380	细胞膜 Cell membrane
Bra029085	BrSMP-4	177	5.43	18 691.81	41.22	82.20	-0.351	细胞膜 Cell membrane
Bra039956	BrSMP-5	262	4.71	26 692.50	34.19	77.21	-0.239	细胞膜 Cell membrane
Bra009983	BrSMP-6	192	4.76	19 473.41	23.22	69.32	-0.515	细胞膜 Cell membrane
Bra036112	BrSMP-7	191	4.99	19 600.77	26.99	75.81	-0.414	细胞核 Nucleus
Bra033375	BrSMP-8	177	4.53	18 185.98	30.21	71.24	-0.540	叶绿体 Chloroplast
Bra033377	BrSMP-9	283	8.89	32 586.25	52.20	75.72	-0.543	叶绿体 Chloroplast