Identification of the VQ Gene Family in Cabbage (Brassica oleracea var. capitata) and Their Expression Analysis in Response to the Infection by Plasmodiophora brassicae
WANG Min, CHEN Jin-Xiu, TAI Xiang, ZHU Xiao-Wei, REN Yun-Ying, BO Tian-Yue*
Institute of Horticulture, Shanghai Academy of Agricultural Science/Shanghai Key Lab of Protected Horticultural Technology, Shanghai 201403, China
Abstract:VQ protein, a class of amino acid sequences containing “FxxxVQxLTG” conservative motifs, is a plant specific protein family, which participated in plant growth, development, and various stress response. In order to clarify the biological function of the VQ gene family in cabbage, 67 BoVQ genes were identified from the whole genome of cabbage, and their bioinformatics and expression patterns were analyzed. The phylogenetic analysis showed that BoVQ genes were divided into 7 subgroups. Chromosomes mapping exhibited BoVQ genes were unevenly distributed in single or cluster on 9 chromosomes of cabbage. The transcriptome data suggested that BoVQ genes expressions varied at different tissues. Eleven BoVQ genes (BoVQ10, BoVQ20, BoVQ22, BoVQ32, BoVQ36, BoVQ43, BoVQ49, BoVQ54, BoVQ59, BoVQ60 and BoVQ67) participated in the whole process of cabbage flower development. The results of real-time fluorescence quantitative PCR (qRT-PCR) showed that BoVQ2, BoVQ12, BoVQ21, BoVQ26 and BoVQ44 genes were significantly high expressed under the infection of clubroot pathogen. Prediction of cis-elements revealed that the pathogen response element W-box and the defense and stress response element TC-rich repeats were enriched in the promoter of BoVQ genes in response to Plasmodiophora brassicae. Protein interaction network prediction showed that there were complex interactions between BoVQ proteins. This study provides a reference for further exploring the function and evolution of BoVQ genes in cabbage.
王敏, 陈锦秀, 邰翔, 朱晓炜, 任云英, 薄天岳. 甘蓝VQ基因家族鉴定及其响应根肿病菌侵染的表达分析[J]. 农业生物技术学报, 2023, 31(9): 1786-1803.
WANG Min, CHEN Jin-Xiu, TAI Xiang, ZHU Xiao-Wei, REN Yun-Ying, BO Tian-Yue. Identification of the VQ Gene Family in Cabbage (Brassica oleracea var. capitata) and Their Expression Analysis in Response to the Infection by Plasmodiophora brassicae. 农业生物技术学报, 2023, 31(9): 1786-1803.
[1] 孙建磊, 董玉梅, 王崇启, 等. 2020. 甜瓜VQ家族基因鉴定及白粉病菌响应分析[J]. 核农学报, 34(11): 2416-2424. (Sun J L, Dong Y M, Wang C Q, et al.2020. Genome-wide identification of the VQ family genes and response of the VQ to powdery mildew infection in melon[J]. Journal of Nuclear Agricultural Sciences, 34(11): 2416-2424.) [2] 邢苗苗, 刘星, 孔枞枞, 等. 2019. 甘蓝NLR家族全基因组鉴定、进化分析及在不同病害胁迫下的表达分析[J]. 园艺学报, 46(4): 723-737. (Xing M M, Liu X, Kong C C, et al.2019. Whole-genome identification and evolutionary analysis of cabbage NLR family genes and their expression profiles in response to various disease stress[J]. Acta Horticulturae Sinica, 46(4): 723-737.) [3] 郑逢盛, 王海华, 邬清韬, 等. 2021. 苦荞VQ基因家族的全基因组鉴定及其在叶斑病原与激素处理下的表达谱分析[J]. 中国农业科学, 54(19): 4048-4060. (Zheng F S, Wang H H, Wu Q T, et al.2021. Genome-wide Identification Of VQ gene family in Fagopyrum tataricum and its expression profiles in response to leaf spot pathogens[J]. Scientia Agricultura Sinica, 54(19): 4048-4060. ) [4] Andreasson E, Jenkins T, Brodersen P, et al.2005. The MAP kinase substrate MKS1 is a regulator of plant defense responses[J]. EMBO Journal, 24(14): 2579-2589. [5] Cai X, Wu J, Liang J, et al.2020. Improved Brassica oleracea JZS assembly reveals significant changing of LTR-RT dynamics in different morphotypes[J]. Theoretical and Applied Genetics, 133(11): 3187-3199. [6] Cao Y P, Meng D D, Abdullah M, et al.2018. Genome wide identification, evolutionary, and expression analysis of VQ genes from two Pyrus species[J]. Genes, 9(4): 224. [7] Chen H, Wang T, He X, et al.2022. BRAD V3.0: An upgraded Brassicaceae database[J]. Nucleic Acids Research, 50(D1): D1432-1441. [8] Cheng Y, Zhou Y, Yang Y, et al.2012. Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors[J]. Plant Physiology, 159(2): 810-825. [9] Chu W Y, Liu B, Wang Y J, et al.2016. Genome-wide analysis of poplar VQ gene family and expression profiling under PEG, NaCl, and SA treatments[J]. Tree Genetics & Genomes, 12(6): 124. [10] Ding H, Yuan G, Mo S, et al.2019. Genome-wide analysis of the plant-specific VQ motif-containing proteins in tomato (Solanum lycopersicum) and characterization of SlVQ6 in thermotolerance[J]. Plant Physiology and Biochemistry, 143: 29-39. [11] Dong Q L, Zhao S, Duan DY, et al.2018. Structural and functional analyses of genes encoding VQ proteins in apple[J]. Plant Science, 272: 208-219. [12] Garrido-Gala J, Higuera J J, Muñoz-Blanco J, et al.2019. The VQ motif-containing proteins in the diploid and octoploid strawberry[J]. Scientific Report, 9: 4942. [13] Guo J, Chen J, Yang J, et al2018. Identification,characterization and expression analysis of the VQ motif-containing gene family in tea plant (Camellia sinensis)[J]. BMC Genomics, 19(1): 710. [14] Jing Y, Lin R.2015. The VQ motif-containing protein family of plant-specific transcriptional regulators[J]. Plant Physiology, 169(1): 371-378. [15] Kim D Y, Kwon S I, Choi C, et al.2013. Expression analysis of rice VQ genes in response to biotic and abiotic stresses[J]. Gene, 529(2): 208-214. [16] Lai Z, Li Y, Wang F, et al.2011. Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense[J]. Plant Cell, 23(10): 3824-3841. [17] Lei R H, Li X L, Ma Z B, et al.2017. Arabidopsis WRKY2 and WRKY34 transcription factors with VQ20 protein to modulate pollen development and function[J]. Plant Journal, 91(6): 962-976. [18] Lescot M, Déhais P, Thijs G, et al.2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences[J]. Nucleic Acids Research, 30(1): 325-327. [19] Li N, Li X, Xiao J, et al.2014a. Comprehensive analysis of VQ motif-containing gene expression in rice defense responses to three pathogens[J]. Plant Cell Report, 33(9): 1493-1505. [20] Li Y L, Jing Y J, Li J J, et al.2014b. Arabidopsis VQ-motif-containing protein 29 represses seedling de-etiolation by interacting with PIF1[J]. Plant physiology, 164(4): 2068-2080. [21] Liu C, Liu H, Zhou C, et al.2020. Genome-wide identification of the VQ protein gene family of tobacco (Nicotiana tabacum L.) and analysis of its expression in response to phytohormones and abiotic and biotic stresses[J]. Genes, 11(3): 284. [22] Livak K J, Schmittgen T.2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta deltaC(T)) method[J]. Methods, 25(4): 402-408. [23] Pan J J, Wang H P, Hu Y R, et al.2018. Arabidopsis VQ18 and VQ26 proteins interact with ABI5 transcription factor to negatively modulate ABA to negatively modulate ABA response during seed germination[J]. The Plant Journal, 95(3): 529-544. [24] Qiu J L, Fiil B K, Petersen K, et al.2008. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus[J]. EMBO Journal, 27(16): 2214-2221. [25] Shan X, Zhang W, Yu F, et al.2019. Genome-wide analysis of basic Helix-Loop-Helix superfamily members reveals organization and chilling-responsive patterns in Cabbage (Brassica oleracea var. capitata L.)[J]. Genes, 10(11): 914. [26] Song W, Zhao H, Zhang X, et al.2016. Genome-wide identification of VQ motif-containing proteins and their expression profiles under abiotic stresses in maize[J]. Frontiers in Plant Science, 6: 1177. [27] Su H, Xing M, Liu X, et al.2019. Genome-wide analysis of HSP70 family genes in cabbage (Brassica oleracea var. capitata) reveals their involvement in floral development[J]. BMC Genomics, 20(1): 369. [28] Wang A, Garcia D, Zhang H, et al.2010. The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis[J]. Plant Journal, 63(4): 670-679. [29] Wang H P, Hu Y R, Pan J J, et al.2015a. Arabidopsis VQ motif-containing proteins VQ12 and VQ29 negatively modulate basal defense against Botrytis cinerea[J]. Scientific Reports, 5: 14185. [30] Wang M, Vannozzi A, Wang G, et al.2015b. A comprehensive survey of the grapevine VQ gene family and its transcriptional correlation with WRKY proteins[J]. Frontiers in Plant Science, 6: 417. [31] Wang X, Zhang H, Sun G, et al.2014. Identification of active VQ motif-containing genes and the expression patterns under low nitrogen treatment in soybean[J]. Gene, 543(2): 237-243. [32] Wang Y B, Jiang Z F, Li Z X, et al.2019. Genome-wide identification and expression analysis of the VQ gene family in soybean (Glycine max)[J]. PeerJ, 21(7): e7509. [33] Wang Y, Liu H, Zhu D, et al.2017. Genome-wide analysis of VQ motif-containing proteins in Moso bamboo (Phyllostachys edulis)[J]. Planta, 246(1): 165-181. [34] Yao Q Y, Xia E H, Liu F H, et al.2015. Genome-wide identification and comparative expression analysis reveal a rapid expansion and functional divergence of duplicated genes in the WRKY gene family of cabbage, Brassica oleracea var. capitata[J]. Gene, 557(1): 35-42. [35] Yuan G, Qian Y, Ren Y, et al.2021. The role of plant-specific VQ motif-containing proteins: An ever-thickening plot[J]. Plant Physiology and Biochemistry, 159(4): 12-16. [36] Zhang G, Wang F, Li J, et al.2015. Genome-wide identification and analysis of the VQ motif-containing protein family in Chinese cabbage (Brassica rapa L. ssp. pekinensis)[J]. International Journal of Molecular Sciences, 16(12): 28683-28704. [37] Zhang G, Wei B.2019. Characterization of VQ motif-containing protein family and their expression patterns under phytohormones and abiotic stresses in melon (Cucumis melo L.)[J]. Plant Growth Regulation, 89: 273-285. [38] Zhang W, Wang S, Yu F, et al.2019. Genome-wide characterization and expression profiling of SWEET genes in cabbage (Brassica oleracea var. capitata L.) reveal their roles in chilling and clubroot disease responses[J]. BMC Genomics, 20(1): 93. [39] Zhong Y, Guo C, Chu J J, et al.2018. Microevolution of the VQ gene family in six species of Fragaria[J]. Genome, 61(1): 49-57. [40] Zou Z, Liu F, Huang S, et al.2020. Genome-wide identification and analysis of VQ motif-containing gene family in Brassica napus and functional characterization of BnMKS1 in response to Leptosphaeria maculans[J]. Phytopathology, 111(2): 281-292.