柑橘U-box基因家族的鉴定及表达分析

doi:10.3864/j.issn.0578-1752.2019.11.009

Abstract

Abstract:

【Objective】 The objectives of this study were to analyze the distribution, structure and evolution of U-box in citrus genome by bioinformatics, to study the expression specificity of family members in different tissues and their responses to abiotic stress and hormones, and to investigate the biological function of U-box gene family in citrus. 【Method】 According to the reported U-box gene of Arabidopsis thaliana, the U-box gene in citrus genome was identified by BLASTp tool in Phytozome database. Phylogenetic tree, subcellular localization prediction, relative mass and isoelectric point and other physical and chemical properties, and scaffold location of U-box member were analyzed with MEGA6.0, Cello, SMART, GSDS2.0, ExPASy and MapChart, respectively. The expression pattern of U-box gene family under low temperature stress was analyzed, and the expression of some members of U-box gene family in citrus treated with NaCl, PEG6000 and different hormones was detected by real-time fluorescence quantitative PCR (qRT-PCR). 【Result】 Fifty-six members of CcPUBs gene family were identified from the whole genome of Citrus clementina, and they could be divided into 7 categories, namely as U-box only, U-box+ARM-1, U-box+WD40-1, TPR+U-box, Kinase+U-box, U-box+ARM-2 and U-box+WD40-2. The theoretical isoelectric point of the family protein was ranged from 5.19 to 9.14, and the number of amino acids encoded was 281 to 1 441. The results of subcellular localization prediction showed that the members of the gene family were located in different positions of the cell, mainly in the nucleus or chloroplast, and a few in the plasma membrane. Cluster analysis showed that citrus U-box was closely related to monocotyledonous rice, and members with the same domain in citrus and Arabidopsis thaliana were clustered together. The results showed that U-box members of citrus had different biological functions, and scaffold localization analysis showed that 56 U-box members were unevenly distributed on citrus 1-9 scaffold. The results of RNA-Seq analysis under cold stress showed that U-box gene family was involved in the response of plants to cold stress and showed four different response patterns. One representative gene was selected respectively from five different clusters of citrus U-box gene family for qRT-PCR analysis. The results showed that CcPUB48 was expressed in all tissues of kumquat, and CcPUB9 and CcPUB4 were mainly expressed in stems and flowers, CcPUB10 was mainly expressed in flowers, stems and young fruits, and CcPUB41 was mainly expressed in leaves and stems. It reflected the tissue-specific expression difference of different U-box members. The expression of CcPUB4, CcPUB10 and CcPUB41 was up-regulated under NaCl stress, but the expression of CcPUB48 had no significant change under salt stress. The expression of CcPUB4 was up-regulated under Na₂CO₃ treatment, which was consistent with that of NaCl treatment, but the expression trend of CaCl₂ treatment was different from that of NaCl treatment. Under the treatment of PEG6000, the expression of CcPUB4 increased at first and then decreased, while CcPUB9, CcPUB41 and CcPUB48 did not change significantly under the treatment of PEG6000. Under gibberellin (GA3) treatment, CcPUB4 was significantly up-regulated at 3 h, while under auxin (IAA) and abscisic acid (ABA), the expression of CcPUB10 showed irregular changes, and the expression of CcPUB10 increased gradually under gibberellin (gibberellin) treatment.【Conclusion】 Fifty-six members of U-box gene were identified from the whole genome of Citrus clementina. All members contained U-box conserved domain and were located in different positions of cells. U-box gene family was involved in the response of plants to cold stress and showed four different response patterns. Under NaCl, PEG6000 and hormone treatment, CcPUB4 and CcPUB10 had different degrees of response, but CcPUB9, CcPUB41 and CcPUB48 had no obvious or no response. This experiment provided a theoretical guidance for the further study of U-box gene family in citrus stress resistance and growth and development mechanism.

Key words: citrus, CcPUB gene family, hormone, stress, gene expression

LI QiuYue,ZHANG YaFei,PENG Jie,WANG Xu,ZHANG ZhiQiang,DAI XiangSheng,JIANG Dong. Genome Wide Identification and Expression Analysis of the U-box Gene Family in Citrus[J].Scientia Agricultura Sinica, 2019, 52(11): 1942-1960.

Figures/Tables 12

Table 1

Table 2

The U-box genes identified in citrus"

基因名称 Gene name	基因组登录号 Gene accession No.	蛋白质大小 Protein length (aa)	分子量 Molecular mass (KD)	等电点 Isoelectric point (PI)	box位置 U-box domain location	细胞定位 Subcellular localizations
CcPUB1	Ciclev10007255m	1380	152.75	5.46	449-513	细胞核 Nuclear
CcPUB2	Ciclev10007527m	769	85.86	6.02	700-762	叶绿体 Chloroplast
CcPUB3	Ciclev10018144m	1088	121.83	6.16	613-677	细胞核 Nuclear
CcPUB4	Ciclev10015253m	444	49.84	8.1	36-100	叶绿体 Chloroplast
CcPUB5	Ciclev10014584m	636	69.48	6.56	257-320	叶绿体 Chloroplast
CcPUB6	Ciclev10014430m	715	78.42	7.01	291-354	叶绿体 Chloroplast
CcPUB7	Ciclev10019643m	537	58.77	6.17	28-91	叶绿体 Chloroplast
CcPUB8	Ciclev10019147m	683	75.51	8.48	279-342	叶绿体 Chloroplast
CcPUB9	Ciclev10032341m	281	31.97	6.03	207-270	细胞质 Cytoplasmic
CcPUB10	Ciclev10024300m	1441	160.62	5.78	506-570	细胞核 Nuclear
CcPUB11	Ciclev10024335m	433	47.91	5.77	79-142	细胞质 Cytoplasmic
CcPUB12	Ciclev10018951m	775	85.47	6.91	239-302	细胞核 Nuclear
CcPUB13	Ciclev10018671m	1008	112.36	5.75	265-328	细胞核 Nuclear
CcPUB14	Ciclev10018795m	888	99.09	5.89	821-884	细胞核 Nuclear
CcPUB15	Ciclev10033932m	687	75.23	6.63	284-347	质膜 Plasma
CcPUB16	Ciclev10030962m	627	68.42	5.49	249-312	叶绿体 Chloroplast
CcPUB17	Ciclev10031496m	456	50.85	8.39	75-138	细胞质 Cytoplasmic
CcPUB18	Ciclev10030608m	1019	113.74	6.24	233-300	细胞核 Nuclear
CcPUB19	Ciclev10030759m	775	86	5.57	282-345	细胞核 Nuclear
CcPUB20	Ciclev10030837m	713	79.13	5.19	220-283	细胞核 Nuclear
CcPUB21	Ciclev10030762m	775	86	5.57	282-345	细胞核 Nuclear
CcPUB22	Ciclev10001406m	395	44.04	6.57	6-69	细胞核 Nuclear
CcPUB23	Ciclev10001380m	398	44.51	8.54	13-76	叶绿体 Chloroplast
CcPUB24	Ciclev10000413m	728	80.97	6.79	248-311	细胞核 Nuclear
CcPUB25	Ciclev10000389m	744	82.67	6.62	264-327	细胞核 Nuclear
CcPUB26	Ciclev10003715m	643	71.66	5.37	274-337	叶绿体 Chloroplast
CcPUB27	Ciclev10000306m	813	89.10	5.38	32-100	细胞核 Nuclear
CcPUB28	Ciclev10011217m	683	74.80	9.14	276-339	叶绿体 Chloroplast
CcPUB29	Ciclev10011844m	416	46.12	8.38	9-74	叶绿体 Chloroplast
CcPUB30	Ciclev10011847m	414	46.93	8.16	12-78	叶绿体 Chloroplast
CcPUB31	Ciclev10011415m	546	59.20	8.42	45-108	叶绿体 Chloroplast
CcPUB32	Ciclev10010958m	1049	118.38	5.48	954-1017	叶绿体 Chloroplast
CcPUB33	Ciclev10011388m	564	64.68	5.22	469-532	细胞质 Cytoplasmic
CcPUB34	Ciclev10011387m	564	64.68	5.22	469-532	细胞质 Cytoplasmic
CcPUB35	Ciclev10011113m	779	88.36	5.43	684-747	叶绿体 Chloroplast
CcPUB36	Ciclev10025062m	679	75.18	5.65	210-273	叶绿体Chloroplast
基因名称 Gene name	基因组登录号 Gene accession No.	蛋白质大小 Protein length (aa)	分子量 Molecular mass (KD)	等电点 Isoelectric point (PI)	box位置 U-box domain location	细胞定位 Subcellular localizations
CcPUB37	Ciclev10024987m	737	81.58	5.84	268-331	叶绿体Chloroplast
CcPUB38	Ciclev10024899m	828	90.51	5.92	239-302	叶绿体Chloroplast
CcPUB39	Ciclev10025589m	450	49.00	7.01	69-132	细胞质Cytoplasmic
CcPUB40	Ciclev10025214m	597	65.21	6.98	39-101	叶绿体Chloroplast
CcPUB41	Ciclev10024952m	760	85.82	6.21	688-751	细胞核Nuclear
CcPUB42	Ciclev10024909m	808	91.47	6.18	736-799	叶绿体Chloroplast
CcPUB43	Ciclev10025637m	435	48.23	8	13-76	质膜Plasma
CcPUB44	Ciclev10028003m	643	71.65	6.54	272-335	叶绿体Chloroplast
CcPUB45	Ciclev10028522m	418	45.74	6.21	17-80	细胞核Nuclear
CcPUB46	Ciclev10028557m	407	45.49	8.78	9-76	叶绿体Chloroplast
CcPUB47	Ciclev10028564m	405	45.68	8.92	9-74	叶绿体Chloroplast
CcPUB48	Ciclev10027966m	661	71.37	5.43	261-324	叶绿体Chloroplast
CcPUB49	Ciclev10028111m	564	60.47	5.46	164-227	叶绿体Chloroplast
CcPUB50	Ciclev10027788m	887	99.83	8.08	820-883	细胞核Nuclear
CcPUB51	Ciclev10029840m	1048	115.56	6.56	265-333	叶绿体Chloroplast
CcPUB52	Ciclev10004235m	1012	112.79	5.91	261-324	叶绿体Chloroplast
CcPUB53	Ciclev10004724m	526	56.90	6.07	1-66	叶绿体Chloroplast
CcPUB54	Ciclev10004393m	757	84.621	5.93	692-754	细胞核Nuclear
CcPUB55	Ciclev10004338m	810	90.50	6.31	745-807	细胞核Nuclear
CcPUB56	Ciclev10006472m	780	88.56	6.55	713-776	叶绿体Chloroplast

Table 2

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Table 3

Cis-acting regulatory elements in promoter of U-box gene family predicted by plantCARE"

顺式元件 Cis-element	典型序列 Typical sequence	特性 Characteristic	基因 Gene
G-box	CACGT	光响应 Cis-acting regulatory element involved in light responsiveness	CcPUB1、CcPUB3—CcPUB11、CcPUB13—CcPUB17、CcPUB21— CcPUB23、CcPUB25、CcPUB26、CcPUB28—CcPUB37、CcPUB39、CcPUB42— CcPUB45、CcPUB47—CcPUB56
ATCT-motif	AATCT	光响应 Part of a conserved DNA module involved in light responsiveness	CcPUB7、CcPUB18、CcPUB22、CcPUB23、CcPUB28、CcPUB30、CcPUB31、CcPUB39、CcPUB53、CcPUB55、CcPUB56
ACE	AAAACGTTTA	光响应 Cis-acting element involved in light responsiveness	CcPUB3、CcPUB10、CcPUB21、CcPUB26、CcPUB32、CcPUB39
LTR	CCGAAA	低温反应 Cis-acting element involved in low- temperature responsiveness	CcPUB2、CcPUB5、CcPUB8、CcPUB10、CcPUB16、CcPUB17、CcPUB23、CcPUB25、CcPUB26、CcPUB28、CcPUB29、CcPUB32、CcPUB38、CcPUB39、CcPUB42—CcPUB44、CcPUB46、CcPUB56
TGACG-motif	TGACG	MeJA响应 Cis-acting regulatory element involved in the MeJA-responsiveness	CcPUB1—CcPUB6、CcPUB8、CcPUB9、CcPUB11、CcPUB13— CcPUB18、CcPUB23、CcPUB27、CcPUB29、CcPUB31—CcPUB38、CcPUB40—CcPUB44、CcPUB46、CcPUB47、CcPUB50、CcPUB52、CcPUB55、CcPUB56
ABRE	GACACGTGGC TACGTG	脱落酸响应 Cis-acting element involved in the abscisic acid responsiveness	CcPUB1—CcPUB11、CcPUB13—CcPUB17、CcPUB22、CcPUB23、CcPUB26、CcPUB28—CcPUB30、CcPUB32—CcPUB37、CcPUB39、CcPUB42—CcPUB45、CcPUB47—CcPUB53、CcPUB55、CcPUB56
GARE-motif	TCTGTTG, AAACAGA	赤霉素响应 Gibberellin-responsive element	CcPUB2、CcPUB5、CcPUB6、CcPUB8、CcPUB9、CcPUB13、CcPUB15、CcPUB16、CcPUB27、CcPUB31、CcPUB45、CcPUB47、
MBS	TAACTG	MYB结合位点参与干旱诱导 MYB binding site involved in drought- induction	CcPUB1、CcPUB4—CcPUB9、CcPUB11、CcPUB14、CcPUB16、CcPUB17、CcPUB21、CcPUB23、CcPUB25—CcPUB27、CcPUB31— CcPUB37、CcPUB39、CcPUB44、CcPUB50、CcPUB51、CcPUB55、CcPUB56
DRE	TGGCCGAC	冷和脱水 Regulatory element involved in cold- and dehydration-responsiveness	CcPUB4、CcPUB5、CcPUB7、CcPUB8、CcPUB13、CcPUB21、CcPUB23、CcPUB26、CcPUB29、CcPUB37、CcPUB40—CcPUB42、CcPUB44、CcPUB46、CcPUB51、CcPUB56
ERE	ATTTTAAA	乙烯响应 Ethylene responsive element	CcPUB2—CcPUB9、CcPUB11、CcPUB12、CcPUB14、CcPUB17、CcPUB18、CcPUB21—CcPUB23、CcPUB25、CcPUB26、CcPUB28、CcPUB29、CcPUB31、CcPUB32、CcPUB37—CcPUB42、CcPUB44、CcPUB45、CcPUB47、CcPUB50—CcPUB53、CcPUB56

Table 3

Fig. 5

Fig. 6

Fig. 7

Fig. 8

Fig. 9

References 37

[1]	SMALLE J, VIERSTRA R D . The ubiquitin 26S proteasome proteolytic pathway. Annual Review of Plant Biology, 2004,55:555-590. doi: 10.1146/annurev.arplant.55.031903.141801 pmid: 15377232
[2]	刘锴栋, 袁长春 . 泛素/26S蛋白酶体途径及其在植物生长发育中的功能. 基因组学与应用生物学, 2009,28(6):1219-1228.
	LIU Y D, YUAN C C . The ubiquitin/26S proteasome pathway and the function in plant development. Genomics and Applied Biology, 2009,28(6):1219-1228. (in Chinese)
[3]	宋素胜, 谢道昕 . 泛素蛋白酶体途径及其对植物生长发育的调控. 植物学通报, 2006,23(5):564-577.
	SONG S S, XIE D X . The ubiquitin-proteosome pathway and plant development. Bulletin of Botany, 2006,23(5):564-577. (in Chinese)
[4]	VANDEMARK A P, HILL C P . Structural basis of ubiquitylation. Current Opinion Structural Biology, 2002,12(6):822-830. doi: 10.1016/S0959-440X(02)00389-5
[5]	HATAKEYAMA S, YADA M, MATSUMOTO M, ISHIDA N, NAKAYAMA K I . U-box proteins as a new family of ubiquitin- protein ligases. The Journal of Biological Chemistry, 2001,276(35):33111-33120. doi: 10.1074/jbc.M102755200
[6]	PATTERSON C . A new gun in town: the U-box is a ubiquitin ligase domain. Science’s STKE, 2002,2002(116): p e4. doi: 10.1126/stke.2002.116.pe4 pmid: 11805346
[7]	FARMER L M, BOOK A J, LEE K H, LIN Y L, FU H, VIERSTRA R D . The RAD23 family provides an essential connection between the 26S proteasome and ubiquitylated proteins in Arabidopsis. The Plant Cell, 2010,22(1):124-142. doi: 10.1105/tpc.109.072660 pmid: 20086187
[8]	VIERSTRA R D . The ubiquitin-26S proteasome system at the nexus of plant biology. Nature Reviews Molecular Cell Biology, 2009,10(6):385-397.
[9]	GONZALEZ -LAMOTHE R, TSITSIGIANNIS D I, LUDWIG A A, PANICOT M, SHIRASU K. JONES J D G , The U-Box protein CMPG1is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell, 2006,18(4):1067-1083. doi: 10.1105/tpc.106.040998
[10]	CHO S K, CHUNG H S, RYU M Y, PARK M J, LEE M M, BAHK Y, KIM J, PAI H S, KIM W T . Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-box E3 ubiquitin ligases homolog. Plant Physiology, 2006,142(4):1664-1682. doi: 10.1104/pp.106.087965
[11]	LIU Y C, WU Y R, HUANG X H, SUN J, XIE Q . AtPUB19, a U-Box E3 ubiquitin ligase, negatively regulates abscisic acid and drought responses in Arabidopsis thaliana. Molecular Plant, 2011,4(6):938-946. doi: 10.1093/mp/ssr030 pmid: 3221247
[12]	HWANG J H, SEO D H, KANG B G, KWAK J M, KIM W T . Suppression of Arabidopsis AtPUB30 resulted in increased tolerance to salt stress during germination. Plant Cell Reports, 2015,34(2):277-289. doi: 10.1007/s00299-014-1706-4
[13]	BRAUMANN I, URBAN W, PREUβ A, DOCKTER C, ZAKHRABEKOVA S, HANSSON M . Semi-dwarf barley (Hordeum vulgare L.) brh2 and ari-l mutants are deficient in a U-box E3 ubiquitin ligase. Plant Growth Regulation, 2018,86(2):223-234. doi: 10.1007/s10725-018-0423-3
[14]	SAMUEL M A, MUDGIL Y, SALT J N, DELMAS F, RAMACHANDRAN S, CHILELLI A, GORING D R . Interactions between the S-Domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiology, 2008,147(4):2084-2095. doi: 10.1104/pp.108.123380
[15]	WU G, TEROL J, IBANEZ V, LOPEZ-GARCIA A, PEREZ-ROMAN E, BORREDA C, DOMINGO C, TADEO F R, CARBONELL- CABALLERO J, ALONSO R, CURK F, DU D, OLLITRAULT P, ROOSE M L, DOPAZO J, GMITTER F G, ROKHSAR D S, TALON M . Genomics of the origin and evolution of Citrus. Nature, 2018,554(7692):311-316. doi: 10.1038/nature25447 pmid: 29414943
[16]	郑兴卫, 邵麟惠, 李聪 . 蒺藜苜蓿全基因组中U-box 基因家族的筛选与特征分析. 草业学报, 2015,24(8):130-141. doi: 10.11686/cyxb2015102
	ZHENG X W, SHAO L H, LI C . Genome-wide screening and characterization of the U-box gene family in Medicago truncatula. Acta Prataculturase Sinica, 2015,24(8):130-141.(in Chinese) doi: 10.11686/cyxb2015102
[17]	WIBORG J, O'SHEA C, SKRIVER K . Biochemical function of typical and variant Arabidopsis thaliana U-box E3 ubiquitin-protein ligases. Biochemical Journal, 2008,413(3):447-457. doi: 10.1042/BJ20071568 pmid: 18393940
[18]	曹英豪 . 水稻U-box基因家族的特征及转录表达模式分析[D]. 保定: 河北农业大学, 2010.
	CAO Y H . The characteristics of Rice U-Box gene family with its transcription and expression pattern analysis[D]. Baoding: Agricultural University of Hebei, 2010.(in Chinese)
[19]	李菲, 何小红, 龚记熠 . 番茄基因组中U-box基因家族的鉴定与分析. 分子植物育种. 2018,16(11):3468-3476
	LI F, HE X H, GONG J Y . Identification and analysis of U-box gene family in tomato genome. Molecular Plant Breeding, 2018,16(11):3468-3476.(in Chinese)
[20]	刘永昌, 曾丽亚, 盘俊, 齐成媚, 袁志辉, 何福林, 胡克坚, 刘小文 . 雷蒙德氏棉Plant U-box(GrPUBs)基因家族生物信息学分析. 分子植物育种, 2018,16(13):4157-4171.
	LIU Y C, ZENG L Y, PAN J, QI C M, YUAN Z H, HE F L, HU K J, LIU X W . Bioinformatics analysis of the plant U-box gene families ( Gr PUBs ) in Gossypium raimondii. Molecular Plant Breeding, 2018,16(13):4157-4171. (in Chinese)
[21]	IGNACIO M . Ancient origin of animal U-box ubiquitin ligases. BMC Evolutionary Biology, 2010,10(1):331. doi: 10.1186/1471-2148-10-331 pmid: 20979629
[22]	CONSORTIUM T T G . The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 2012,485(7400):635. doi: 10.1038/nature11119
[23]	LUO J, SHEN G, YAN J, HE C, ZHANG H . AtCHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment. The Plant Journal, 2006,46(4):649-657. doi: 10.1111/tpj.2006.46.issue-4
[24]	ADLER G, KONRAD Z, ZAMIR L, MISHRA A K, RAVEH D, BAR-ZVI D . The Arabidopsis paralogs,PUB46 and PUB48, encoding U-box E3 ubiquitin ligases, are essential for plant response to drought stress. BMC Plant Biology, 2017,17(1):8. doi: 10.1186/s12870-016-0963-5
[25]	BERGLER J, HOTH S . Plant U-box armadillo repeat proteins AtPUB18 and AtPUB19 are involved in salt inhibition of germination in Arabidopsis. Plant Biology, 2011,13(5):725-730. doi: 10.1111/plb.2011.13.issue-5
[26]	SADANANDOM A . The U-box protein AtPUB17 is a functional ortholog of NtACRE276 and its E3 ubiquitin ligase activity is required for plant cell death and defence. Comparative Biochemistry & Physiology Part A, 2007,146(4):S203-S203.
[27]	SANKARANARAYANAN S, SAMUEL M A . A proposed role for selective autophagy in regulating auxin-dependent lateral root development under phosphate starvation in Arabidopsis. Plant Signaling & Behavior, 2015,10(3):e989749.
[28]	齐晨辉, 赵先炎, 韩朋良 . 苹果U-box型E3泛素连接酶MdPUB24的耐盐性和ABA敏感性鉴定. 园艺学报, 2017,44(12):2255-2264.
	QI C H, ZHAO X Y, HAN P L . Functional identification of salt tolerance and ABA sensitivity of apple U-box E3 ubiquitin ligase MdPUB24. Acta Horticulturae Sinica, 2017,44(12):2255-2264. (in Chinese)
[29]	LIU J, LI W, NING Y, SHIRSEKAR G, CAI Y, WANG X, DAI L, WANG Z, LIU W, WANG G L . The U-Box E3 ligase SPL11/PUB13 is a convergence point of defense and flowering signaling in plants. Plant Physiology, 2012,160(1):28-37. doi: 10.1104/pp.112.199430
[30]	SHARMA M, PANDEY G K . Expansion and function of repeat domain proteins during stress and development in plants. Frontiers in Plant Science, 2016,6:1218.
[31]	SANTNER A, CALDERON-VILLALOBOS L I A, ESTELLE M . Plant hormones are versatile chemical regulators of plant growth. Nature Chemical Biology, 2009,5(5):301-307. doi: 10.1038/nchembio.165 pmid: 19377456
[32]	HWANG J H, DONG H S, KANG B G, KWAK J M, KIM W T . Suppression of Arabidopsis, AtPUB30, resulted in increased tolerance to salt stress during germination. Plant Cell Reports, 2015,34(2):277-289. doi: 10.1007/s00299-014-1706-4
[33]	CHO S K, CHUANG H S, RYU M Y, PARK M J, LEE M M, BAHK Y, KIM J, PAI H S, KIM W T . Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-Box E3 ubiquitin ligase homolog. Plant Physiology, 2006,142(4):1664-1682. doi: 10.1104/pp.106.087965
[34]	KOBAYASHI S, TSUGAMA D, LIU S, TAKANO T . A U-Box E3 ubiquitin ligase, PUB20, interacts with the Arabidopsis G-Protein β subunit, AGB1. PLoS ONE, 2012,7(11):e49207. doi: 10.1371/journal.pone.0049207
[35]	SEO D H, RYU M Y, JAMMES F, HWANG J H, TUREK M, KANG B G, KWAK J M, KIM W T . Roles of Four Arabidopsis U-Box E3 ubiquitin ligases in negative regulation of abscisic acid-mediated drought stress responses. Plant Physiology, 2012,160(1):556-568. doi: 10.1104/pp.112.202143
[36]	YEE D, GORING D R . The diversity of plant U-box E3 ubiquitin ligases: From upstream activators to downstream target substrates. Journal of Experimental Botany, 2009,60(4):1109-1121. doi: 10.1093/jxb/ern369 pmid: 19196749
[37]	WANG M, ZHANG X, LIU J H . Deep sequencing-based characterization of transcriptome of trifoliate orange (Poncirus trifoliata (L.) Raf.) in response to cold stress. BMC Genomics, 2015,16(1):555. doi: 10.1186/s12864-015-1629-7

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引物名称 Primer name	正向引物序列 Forward primer sequence	反向引物序列 Reverse primer sequence
CcPUB4	CCGGTGACTTTATCCACTGGG	GAATGGGTTCAAAACTCGTCAGG
CcPUB9	GCCAGCTGAGGTCCCGGATT	TGCCTTGTATGCCCAACCATGT
CcPUB10	CAAAACCCGTAGTCCGAAAA	AATTCACCATCCGAGTCTGC
CcPUB41	ACGCCGTCCAGTATCCTTC	AATTCCAGCATTCCCATCCA
CcPUB48	CTGAGCGAAGGTACCAGAG	AGTGTTCATCCACCATTCC
β-Actin	CCCCATCGTTACCGTCCAG	CGCCTTGCCAGTTGAATATCC

Genome Wide Identification and Expression Analysis of the U-box Gene Family in Citrus

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