Genome-wide Identification and Expression Analysis of Tomato BURP Structural Domain Gene Family

doi:10.13304/j.nykjdb.2023.0311

Abstract

Abstract:

BURP domain proteins are unique to plants and play different roles in plant stress， growth and development. To identify BURP domain genes （SlBURP） and their expression in tomato， a total of 12 SlBURP genes were identified in tomato. The phylogenetic analysis classified 12 SlBURP genes into 7 subfamilies， which had significant differences in conserved motifs and gene structures among the different subfamilies. The extensive presence of stress， growth， hormone， and light-responsive elements in the promoter sequences of SlBURPs suggested that this family had crucial role in abiotic stress. Covariance analysis indicated that members of tomato and ArabidopsisBURP gene families were derived from the same ancestor. The RT-qPCR results showed that the expression levels of SlBURP6， SlBURP7， SlBURP8 and SlBURP12 were abundantly in leaves； the expression levels of SlBURP2， SlBURP6， SlBURP7 and SlBURP8 increased after salt treatment； the expression levels of SlBURP5， SlBURP8， SlBURP9 and SlBURP12 increased during fruit development under plant regulator treatment. In summary， SlBURP genes played important roles in both stress and growth of tomato.

Key words: tomato, BURP gene family, fruit development, salt stress, expression analysis

摘要：

BURP结构域蛋白为植物所特有，在植物生长发育和胁迫响应中起着重要作用。为鉴定番茄BURP结构域基因（SlBURP）及分析其表达，从番茄基因组中鉴定出12个SlBURP基因，系统进化分析将其分为7个亚族，不同亚族的保守基序和基因结构有明显差异。SlBURPs启动子序列中广泛存在胁迫、生长、激素、光响应元件，表明该家族基因在对非生物胁迫的响应中有重要作用。共线性分析表明，番茄SlBURP基因和拟南芥BURP基因家族成员来自同一祖先。RT-qPCR表明，SlBURP6、SlBURP7、SlBURP8、SlBURP12在叶中大量表达；SlBURP2、SlBURP6、SlBURP7、SlBURP8在盐处理后转录水平上升；在植物调节剂处理下SlBURP5、SlBURP8、SlBURP9、SlBURP12基因在果实发育期的转录水平均有上升。综上所述，SlBURP基因在番茄生长发育和逆境胁迫中起着重要作用。

关键词: 番茄, BURP基因家族, 果实发育, 盐胁迫, 表达分析

CLC Number:

S641.2

Fulin ZHANG, Rui XI, Yuxiang LIU, Zhaolong CHEN, Qinghui YU, Ning LI. Genome-wide Identification and Expression Analysis of Tomato BURP Structural Domain Gene Family[J]. Journal of Agricultural Science and Technology, 2024, 26(8): 51-62.

张福林, 奚瑞, 刘宇翔, 陈兆龙, 余庆辉, 李宁. 番茄BURP结构域基因家族全基因组鉴定及表达分析[J]. 中国农业科技导报, 2024, 26(8): 51-62.

Figures/Tables 11

References 37

1	PHILLIPS K, LUDIDI N. Drought and exogenous abscisic acid alter hydrogen peroxide accumulation and differentially regulate the expression of two maize RD22-like genes [J/OL]. Sci. Rep., 2017, 7(1):8821 [2023-07-31]. .
2	VAN SON L, TIEDEMANN J, RUTTEN T, et al.. The BURP domain protein AtUSPL1 of Arabidopsis thaliana is destined to the protein storage vacuoles and overexpression of the cognate gene distorts seed development [J]. Plant Mol. Biol., 2009, 71(4):319-329.
3	JIN J, JEMAA E, XU Z, et al.. Arabidopsis ETHYLENE INSENSITIVE 3 directly regulates the expression of PG1β-like family genes in response to aluminum stress [J/OL]. J. Exp. Bot., 2022, 14:161 [2023-07-31]. .
4	DING X P, HOU X, XIE K B, et al.. Genome-wide identification of BURP domain-containing genes in rice reveals a gene family with diverse structures and responses to abiotic stresses [J]. Planta, 2009, 230(1):149-163.
5	KOMATSU S, NANJO Y, NISHIMURA M. Proteomic analysis of the flooding tolerance mechanism in mutant soybean [J]. J. Proteomics, 2013, 79:231-250.
6	TANG Y L, LI X J, ZHONG Y T, et al.. Functional analysis of soybean SALI3-2 in yeast [J]. Shenzhen Univ. Sci. Eng., 2007, 24:324-330.
7	GAN D, JIANG H, ZHANG J, et al.. Genome-wide analysis of BURP domain-containing genes in maize and sorghum [J]. Mol. Biol. Rep., 2011, 38(7):4553-4563.
8	YU S W, ZHANG L D, ZUO K J, et al.. Isolation and characterization of a BURP domain-containing gene BnBDC1 from Brassica napus involved in abiotic and biotic stress [J]. Physiol. Plantarum, 2004, 122(2):210-218.
9	THAMMEGOWDA H V, LE V S, CHRISTIANE S, et al.. AtRD22 and AtUSPL 1, members of the plant-specific BURP domain family involved in Arabidopsis thaliana drought tolerance [J/OL]. PLoS One, 2014, 9(10):e110065 [2023-07-31]. .
10	TEERAWANICHPAN P, XIA Q, CALDWELL S J, et al.. Protein storage vacuoles of Brassica napus zygotic embryos accumulate a BURP domain protein and perturbation of its production distorts the PSV [J]. Plant Mol. Biol., 2009, 71(4):331-343.
11	WANG A M, XIA Q, XIE W S, et al.. The classical ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development [J]. Proc. Natl. Acad. Sci. USA, 2003, 100:14487-14492.
12	XU X Y, YANG H K, SINGH S P, et al.. Genetic manipulation of non-classic oilseed plants for enhancement of their potential as a biofactory for triacylglycerol production [J/OL]. Engineering, 2018, 4(4):11 [2023-07-31]. .
13	XU B, GOU J Y, LI F G, et al.. A cotton BURP domain protein interacts with α‍-expansin and their co-expression promotes plant growth and fruit production [J]. Mol. Plant, 2013, 6(3):945-958.
14	MATUS J T, AQUEA F, ESPINOZA C, et al.. Inspection of the grapevine BURP superfamily highlights an expansion of RD22 genes with distinctive expression features in berry development and ABA-mediated stress responses [J/OL]. PLoS One, 2014, 9(10):e110372 [2023-07-31]. .
15	宋单单,史梦雪,高金汇,等.复配型转光棚膜光学性能及其对日光温室番茄生长及果实品质的影响[J].植物生理学报,2022,58(11):2218-2226.
	SONG D D, SHI M X, GAO J H, et al.. Optical properties of complex-type of light conversion greenhouse films and their effects on the growth and fruit qualities of tomato in solar greenhouse [J]. J. Plant Physiol., 2022, 58(11):2218-2226.
16	刘向蕾,尹亚红,高玉迪,等.番茄SlNPF68基因参与缺氮条件下根系觅食反应[J].植物生理学报,2022,58(7):1212-1220.
	LIU X L, YIN Y H, GAO Y D, et al.. SlNPF68 gene involved in root foraging response under nitrogen deficiency in tomato [J]. J. Plant Physiol., 2022, 58(7):1212-1220.
17	万玉通,裴茂松,韦同路,等.甲基化修饰影响果实生长发育的研究进展[J].植物生理学报,2022,57(3):531-541.
	WAN Y T, PEI M S, WEI T L, et al.. Progress of methylation modification on fruit development [J]. J. Plant Physiol., 2022, 57(3):531-541.
18	SUN H R, WEI H L, WANG H T, et al.. Genome-wide identification and expression analysis of the BURP domain-containing genes in Gossypium hirsutum [J/OL]. BMC Genomics, 2019, 20:558 [2023-07-31]. .
19	XU H, LI Y, YAN Y, et al.. Genome-scale identification of soybean BURP domain-containing genes and their expression under stress treatments [J]. BMC Plant Biol., 2010, 10(1):1-16.
20	JEONG H Y, NGUYEN H P, EOM S H, et al.. Integrative analysis of pectin methylesterase (PME) and PME inhibitors in tomato (Solanum lycopersicum): identification, tissue-specific expression, and biochemical characterization [J]. Plant Physiol. Biochem., 2018, 132:557-565.
21	XU Q, DUNBRACK R L. Assignment of protein sequences to existing domain and family classification systems: Pfam and the PDB [J]. Bioinformatics, 2012, 28(21):2763-2772.
22	SONNHAMMER E, EDDY S R, DURBIN R. Pfam: a comprehensive database of protein domain families based on seed alignments [J]. Proteins, 2015, 28(3):405-420.
23	SCHULTZ J, COPLEY R R, TOBIAS D, et al.. SMART: a web-based tool for the study of genetically mobile domains [J]. Nucl. Acids Res., 2000, 28:231-234.
24	ARTIMO P, JONNALAGEDDA M, ARNOLD K, et al.. ExPASy: SIB bioinformatics resource portal [J]. Nucl. Acids Res.. 2012, 40:597-603.
25	HORTON P, PARK K J, OBAYASHI T, et al.. WoLF PSORT: protein localization predictor [J]. Nucl. Acids Res., 2007, 35:585-587.
26	KUMAR S, STECHER G, TAMURA K. MEGA7 molecular evolutionary genetics analysis version 7.0 for bigger datasets [J]. Mol. Biol. Evol., 2015, 33:1870-1874.
27	CHEN C, CHEN H, ZHANG Y, et al.. TBtools: an integrative toolkit developed for interactive analyses of big biological data [J/OL]. Mol. Plant, 2020, 13(8):009 [2023-07-31] .
28	ROMBAUTS, DEHAIS, MONTAGU V, et al.. PlantCARE, a plant cis-acting regulatory element database [J]. Nucl. Acids Res., 1999, 27:295-296.
29	LIVAK K J, SCHMITTGEN T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2^- ^ΔΔ ^CT [J]. Methods, 2001, 25:492-508.
30	张中保,吴忠义,魏建华.玉米BURP家族基因的鉴定和分析[J].玉米科学,2014,22(3):36-42.
	ZHANG Z B, WU Z Y, WEI J H. Genome-wide analysis and identification of ZmBURP genes family in maize [J]. J. Maize Sci., 2014, 22(3):36-42.
31	SHAO Y H, WEI G, WANG L, et al.. Genome-wide analysis of BURP domain-containing genes in Populus trichocarpa [J]. J. Integr. Plant Biol., 2011, 53(9):743-755.
32	GRANGER C, CORYELL V, KHANNA A, et al.. Identification, structure, and differential expression of members of a BURP domain containing protein family in soybean [J/OL]. Genome, 2002, 45(4):693 [2023-07-31]. .
33	LI Y, CHEN X, CHEN Z, et al.. Identification and expression analysis of BURP domain-containing genes in Medicago truncatula [J/OL]. Front. Plant Sci., 2016, 7:485 [2023-07-31]. .
34	YU S W, ZHANG L D, ZUO K J, et al.. Isolation and characterization of a BURP domain-containing gene BnBDC1 from Brassica napus involved in abiotic and biotic stress [J]. Physiol. Plantarum, 2004, 100:210-218.
35	WANG H M, ZHOU L, FU Y P, et al.. Expression of an apoplast-localized BURP-domain protein from soybean (GmRD22) enhances tolerance towards abiotic stress [J]. Plant Cell Environ., 2012, 35(11):1932-4197.
36	米子岚,钟活权,江年琼,等.BURP蛋白家族与植物对非生物胁迫的响应[J].中国细胞生物学学报,2015, 37(9):1302-1308.
	MI Z L, ZHONG H Q, JIANG N Q, et al.. BURP Proteins Family and the Response of Plant to Abiotic Stress [J]. J. Cell Biol., 2015, 37(9):1302-1308.
37	WANG L H, WU N N, ZHU Y, et al.. The divergence and positive selection of the plant-specific BURP-containing protein family [J]. Ecol. Evol., 2015, 5(22):5394-5412.

处理 Treatment	试剂 Reagent
CK	蒸馏水Distilled water
EBR0.05	0.05 mg·L^-1 EBR
EBR0.10	0.10 mg·L^-1 EBR
EBR0.20	0.20 mg·L^-1 EBR
MT50	50 μmol·L^-1 MT
MT100	100 μmol·L^-1 MT
MT150	150 μmol·L^-1 MT
NAA10	10 mg·L^-1 NAA
NAA20	20 mg·L^-1 NAA
NAA30	30 mg·L^-1 NAA

处理 Treatment	试剂 Reagent
CK	蒸馏水Distilled water
EBR0.05	0.05 mg·L^-1 EBR
EBR0.10	0.10 mg·L^-1 EBR
EBR0.20	0.20 mg·L^-1 EBR
MT50	50 μmol·L^-1 MT
MT100	100 μmol·L^-1 MT
MT150	150 μmol·L^-1 MT
NAA10	10 mg·L^-1 NAA
NAA20	20 mg·L^-1 NAA
NAA30	30 mg·L^-1 NAA

基因名称 Gene name	正向引物序列 Forward primer sequence （5’-3’）	反向引物序列 Reverse primer sequence （5’-3’）
SlBURP2	GCGGAGGCAATGCTTGATT	GCCACCATCTTGGGAGTTTCTA
SlBURP3	CGGTGTTGATGGAACTAAGGTG	TGACAAATAGAGGGAGCACCAG
SlBURP5	ACAGAGGAAGAGATTCGTGAGC	GAAGGGAATGGTTGATTGGC
SlBURP6	GCAATGCGTGGCGTCTATT	TGATTTCGTCACTCTTCCGC
SlBURP7	GGCAATACGCCTGTCCAAA	GACCAGCATTTCCATCGTTTC
SlBURP8	GGTCGTAATGTGGTGGTTCG	CGCTTCGTAGACTCGGACTTT
SlBURP9	GGTGAGACGAAACGATGTGTT	CCACCGTTGATTCCTTTGACT
SlBURP10	AGACGGTGTTGTTCCTGAGC	GTATCGTTGGGATGCTTGAGTT
SlBURP11	TCAAGCCAAGGTCTATCCAGC	AATGAGCGATGAGGGAACG
SlBURP12	GTTGGAGGCAATAAAGGCG	AACAAACGGTGAGGGTCCA
SlActin	CAGGGTGTTCTTCAGGAGCAA	GGTGTTATGGTCGGAATGGG

基因名称 Gene name	正向引物序列 Forward primer sequence （5’-3’）	反向引物序列 Reverse primer sequence （5’-3’）
SlBURP2	GCGGAGGCAATGCTTGATT	GCCACCATCTTGGGAGTTTCTA
SlBURP3	CGGTGTTGATGGAACTAAGGTG	TGACAAATAGAGGGAGCACCAG
SlBURP5	ACAGAGGAAGAGATTCGTGAGC	GAAGGGAATGGTTGATTGGC
SlBURP6	GCAATGCGTGGCGTCTATT	TGATTTCGTCACTCTTCCGC
SlBURP7	GGCAATACGCCTGTCCAAA	GACCAGCATTTCCATCGTTTC
SlBURP8	GGTCGTAATGTGGTGGTTCG	CGCTTCGTAGACTCGGACTTT
SlBURP9	GGTGAGACGAAACGATGTGTT	CCACCGTTGATTCCTTTGACT
SlBURP10	AGACGGTGTTGTTCCTGAGC	GTATCGTTGGGATGCTTGAGTT
SlBURP11	TCAAGCCAAGGTCTATCCAGC	AATGAGCGATGAGGGAACG
SlBURP12	GTTGGAGGCAATAAAGGCG	AACAAACGGTGAGGGTCCA
SlActin	CAGGGTGTTCTTCAGGAGCAA	GGTGTTATGGTCGGAATGGG

基因ID Gene ID	基因名称 Gene name	染色体 Chromosome	氨基酸数量 Number of amino acids	分子量 Molecular weight/Da	等电点 pI	脂肪指数 Aliphatic index	亲水性 Hydrophilicity	亚细胞定位 Subcellular localization
Solyc01g004131.1	SlBURP1	1	813	92 342.76	6.17	79.68	-0.299	叶绿体Chloroplast
Solyc01g004134.1	SlBURP2	1	1 200	131 593.70	8.28	57.20	-0.589	叶绿体Chloroplast
Solyc02g000714.2	SlBURP3	2	365	39 549.89	7.26	73.04	-0.438	胞外Extracellular
Solyc02g000715.1	SlBURP4	2	405	45 924.69	6.09	75.11	-0.547	细胞质Cytoplasmic
Solyc02g000716.1	SlBURP5	2	264	30 034.04	7.10	87.54	-0.031	胞外Extracellular
Solyc03g002688.1	SlBURP6	3	322	36 324.05	8.54	84.72	-0.248	细胞核Nucleus
Solyc05g000048.2	SlBURP7	5	337	38 173.93	7.65	84.69	-0.217	细胞核Nucleus
Solyc05g000050.1	SlBURP8	5	325	37 217.51	6.05	76.46	-0.303	胞外Extracellular
Solyc05g000051.1	SlBURP9	5	611	66 805.31	6.16	51.72	-0.689	细胞核Nucleus
Solyc05g001003.1	SlBURP10	5	629	69 069.40	7.93	58.46	-0.632	胞外Extracellular
Solyc06g002169.1	SlBURP11	6	693	76 193.18	9.22	61.07	-0.470	叶绿体Chloroplast
Solyc08g001592.1	SlBURP12	8	408	45 869.40	9.02	76.45	-0.262	细胞质Cytoplasmic