Genome-wide identification of WD40 superfamily genes and prediction of WD40 gene of flavonoid-related genes in Ginkgo biloba

Authors

  • Jiarui ZHENG Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Yongling LIAO Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Feng XU Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Xian ZHOU Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Jiabao YE Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Mingyue FU Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Xiaomeng LIU Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Zhengyan CAO Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Weiwei ZHANG Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)

DOI:

https://doi.org/10.15835/nbha49212086

Keywords:

flavonoid, genome, Ginkgo biloba, superfamily genes, WD40

Abstract

The WD40 transcription factor family is a superfamily found in eukaryotes and implicated in regulating growth and development. In this study, 167 WD40 family genes are identified in the Ginkgo biloba genome. They are divided into 5 clusters and 16 subfamilies based on the difference analysis of a phylogenetic tree and domain structures. The distribution of WD40 genes in chromosomes, gene structures, and motifs is analyzed. Promoter analysis shows that five GbWD40 gene promoters contain the MYB binding site participating in the regulation of flavonoid metabolism, suggesting that these five genes may participate in the regulation of flavonoid synthesis in G. biloba. The correlation analysis is carried out based on FPKM value of WD40 gene and flavonoid content in 8 tissues of G. biloba. Six GbWD40 genes that may participate in flavonoid metabolism are screened. The biological functions of the WD40 family genes in G. biloba are systematically analyzed, providing a foundation for further elucidating their regulatory mechanisms. A number of WD40 candidate genes involved in the biosynthesis and metabolism of G. biloba also predicted. This study presents an important basis and direction for conducting further research on the regulatory network of flavonoid synthesis and metabolism.

References

Albert NW, Thrimawithana AH, McGhie TK, Clayton WA, Deroles SC, Schwinn KE, … Davies KM (2018). Genetic analysis of the liverwort Marchantia polymorpha reveals that R2R3-MYB activation of flavonoid production in response to abiotic stress is an ancient character in land plants. New Phytologist 218(2):554-566. https://doi.org/10.1111/nph.15002

Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, … Noble WS (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research 37:W202-W208. https://doi.org/10.1093/nar/gkp335

Carey CC, Strahle JT, Selinger DA, Chandler VL (2004). Mutations in the pale aleurone color1 regulatory gene of the Zea mays anthocyanin pathway have distinct phenotypes relative to the functionally similar TRANSPARENT TESTA GLABRA1 gene in Arabidopsis thaliana. Plant Cell 16(2):450-464. https://doi.org/10.1105/tpc.018796

Chen C, Chen H, Zhang Y, Thomas Hannah R, Frank Margaret H, He Y, Xia R (2020). TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13(8):1194-1202. https://doi.org/10.1016/j.molp.2020.06.009

Chen S, Wang S (2019). GLABRA2, a common regulator for epidermal cell fate determination and anthocyanin biosynthesis in Arabidopsis. International Journal of Molecular Sciences 20(20):4997. https://doi.org/10.3390/ijms20204997

Danino YM, Even D, Ideses D, Juven-Gershon T (2015). The core promoter: at the heart of gene expression. Biochimica et Biophysica Acta-Gene Regulatory Mechanisms 1849(8):1116-1131. https://doi.org/10.1016/j.bbagrm.2015.04.003

El-Gebali Sara, Mistry Jaina, Bateman Alex, Eddy Sean R, Luciani Aurelien, Potter Simon C, … Finn Robert D (2019). The Pfam protein families database in 2019. Nucleic Acids Research 47(8):D427-D432. https://doi.org/10.1093/nar/gky995

Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007). Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant Journal 49(3):414-427. https://doi.org/10.1111/j.1365-313X.2006.02964.x

Feng R, Zhang C, Ma R, Cai Z, Lin Y, Yu M (2019). Identification and characterization of WD40 superfamily genes in peach. Gene 710:291-306. https://doi.org/10.1016/j.gene.2019.06.010

Feyissa BA, Arshad M, Gruber MY, Kohalmi SE, Hannoufa A (2019). The interplay between miR156/SPL13 and DFR/WD40–1 regulate drought tolerance in alfalfa. BMC Plant Biology 19:434. https://doi.org/10.1186/s12870-019-2059-5

Gong W, Chen C, Dobes C, Fu CX, Koch MA (2008). Phylogeography of a living fossil: Pleistocene glaciations forced Ginkgo biloba L. (Ginkgoaceae) into two refuge areas in China with limited subsequent postglacial expansion. Molecular Phylogenetics and Evolution 48(3):1094-1105. https://doi.org/10.1016/j.ympev.2008.05.003

Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW (2011). Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23(4):1512-1522. https://doi.org/10.1105/tpc.111.084525

Guan R, Zhao Y, Zhang H, Fan G, Liu X, Zhou W, … Chen W (2019). Updated genome assembly of Ginkgo biloba GigaScience database. Gigascience 2019. http://dx.doi.org/10.5524/100613

Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V (2011). Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. Journal of Experimental Botany 62(8):2465-2483. https://doi.org/10.1093/jxb/erq442

Hong Y, Tang X, Huang H, Zhang Y, Dai S (2015). Transcriptomic analyses reveal species-specific light-induced anthocyanin biosynthesis in chrysanthemum. BMC Genomics 16(1):202. https://doi.org/10.1186/s12864-015-1428-1

Hu XJ, Li T, Wang Y, Xiong Y, Wu XH, Zhang DL, … Wu YD (2017). Prokaryotic and highly-repetitive WD40 proteins: a systematic study. Scientific Reports 7(1):10585. https://doi.org/10.1038/s41598-017-11115-1

Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015). GSDS 2.0: an upgraded gene features visualization server. Bioinformatics 31(8): 1296-1297. https://doi.org/10.1093/bioinformatics/btu817

Hu R, Xiao J, Gu T, Yu XF, Zhang Y, Chang JL, … He GY (2018). Genome-wide identification and analysis of WD40 proteins in wheat (Triticum aestivum L.). BMC Genomics 19(1): 803. https://doi.org/10.1186/s12864-018-5157-0

Jain BP, Pandey S (2018). WD40 repeat proteins: signalling scaffold with diverse functions. Protein Journal 37(5):391-406. https://doi.org/10.1007/s10930-018-9785-7

Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, … Rombauts S (2002). PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30(1):325-327. https://doi.org/10.1093/nar/30.1.325

Li S (2014). Transcriptional control of flavonoid biosynthesis: fine-tuning of the MYB-bHLH-WD40 (MBW) complex. Plant Signaling Behavior 9(1):e27522. https://doi.org/10.4161/psb.27522

Liu H, Cao F, Yin T, Chen Y (2017). A highly dense genetic map for Ginkgo biloba constructed using sequence-based markers. Frontiers in Plant Science 8: 1041. https://doi.org/10.3389/fpls.2017.01041

Lin XH, Zhang J, Li Y, Luo HM, Wu Q, Sun C, … Chen S (2011). Functional genomics of a living fossil tree, Ginkgo, based on next-generation sequencing technology. Physiologia Plantarum 143(3):207-218. https://doi.org/10.1111/j.1399-3054.2011.01500.x

Liu Z, Liu YH, Coulter AJ, Shen BY, Li YM, Li CZ, … Zhang JL (2020). The WD40 gene family in potato (Solanum Tuberosum L.): genome-wide analysis and identification of anthocyanin and drought-related WD40s. Agronomy 10(3):401. https://doi.org/10.3390/agronomy10030401

Migliori V, Mapelli M, Guccione E (2012). On WD40 proteins: propelling our knowledge of transcriptional control?. Epigenetics 7(8):815-822. https://doi.org/10.4161/epi.21140

Nakatsuka T, Haruta KS, Pitaksutheepong C, Abe Y, Kakizaki Y, Yamamoto K, … Nishihara M (2008). Identification and characterization of R2R3-MYB and bHLH transcription factors regulating anthocyanin biosynthesis in gentian flowers. Plant and Cell Physiology 49(12):1818-1829. https://doi.org/10.1093/pcp/pcn163

Ni J, Dong LX, Jiang ZF, Yang XL, Chen ZY, Wu YH, Xu MJ (2018). Comprehensive transcriptome analysis and flavonoid profiling of Ginkgo leaves reveals flavonoid content alterations in day-night cycles. PLoS One 13(3):e0193897. https://doi.org/10.1371/journal.pone.0193897

Ouyang Y, Huang X, Lu Z, Yao J (2012). Genomic survey, expression profile and co-expression network analysis of OsWD40 family in rice. BMC Genomics 13:100. https://doi.org/10.1186/1471-2164-13-100

Pesch M, Schultheiss I, Klopffleisch K, Uhrig JF, Koegl M, Clemen CS, … Hulskamp M (2015). Transparent testa GLABRA1 and GLABRA1 compete for binding to GLABRA3 in Arabidopsis. Plant Physiology 168(2):584-597. https://doi.org/10.1104/pp.15.00328

Ponting CP, Schultz J, Milpetz F, Bork P (1999). SMART: identification and annotation of domains from signalling and extracellular protein sequences. Nucleic Acids Research 27(1):229-232. https://doi.org10.1093/nar/27.1.229

Salih H, Gong W, Mkulama M, Du X (2018). Genome-wide characterization, identification, and expression analysis of the WD40 protein family in cotton. Genome 61(7):539-547. https://doi.org/10.1139/gen-2017-0237

Suganuma T, Pattenden SG, Workman JL (2008). Diverse functions of WD40 repeat proteins in histone recognition. Genes Development 22(10):1265-1268. https://doi.org/10.1101/gad.1676208

Stirnimann CU, Petsalaki E, Russell RB, Müller CW (2010). WD40 proteins propel cellular networks. Trends in Biochemical Sciences 35(10):565-574. https://doi.org/10.1016/j.tibs.2010.04.003

Sun YB, Zhang XJ, Zhong MC, Dong X, Yu DM, Jiang XD, … Hu JY (2020). Genome-wide identification of WD40 genes reveals a functional diversification of COP1-like genes in Rosaceae. Plant Molecular Biology 104(1-2):81-95. https://doi.org/10.1007/s11103-020-01026-7

Ude C, Schubert-Zsilavecz M, Wurglics M (2013). Ginkgo biloba extracts: a review of the pharmacokinetics of the active ingredients. Clinical Pharmacokinetics 52(9):727-749. https://doi.org/10.1007/s40262-013-0074-5

van Nocker S, Ludwig P (2003). The WD-repeat protein superfamily in Arabidopsis: conservation and divergence in structure and function. BMC Genomics 4(1):50. https://doi.org/10.1186/1471-2164-4-50

Wu Y, Guo J, Zhou Q, Xin Y, Wang G, Xu LA (2018). De novo transcriptome analysis revealed genes involved in flavonoid biosynthesis, transport and regulation in Ginkgo biloba. Industrial Crops and Products 124:226-235. https://doi.org/10.1016/j.indcrop.2018.07.060

Winkel-Shirley B (2001). Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126(2):485-493. https://doi.org/10.1104/pp.126.2.485

Xie Y, Tan H, Ma Z, Huang J (2016). Della proteins promote anthocyanin biosynthesis via sequestering MYBL2 and JAZ suppressors of the MYB/bHLH/WD40 complex in Arabidopsis thaliana. Molecular Plant 9(5):711-721. https://doi.org/10.1016/j.molp.2016.01.014

Xu F, Ning YJ, Zhang WW, Liao YL, Li LL, Cheng H, Cheng SY (2014). An R2R3-MYB transcription factor as a negative regulator of the flavonoid biosynthesis pathway in Ginkgo biloba. Functional Integrative Genomics 14(1):177-189. https://doi.org/10.1007/s10142-013-0352-1

Xu C, Min J (2011). Structure and function of WD40 domain proteins. Protein Cell 2(3):202-214. htpps://doi.org/10.1007/s13238-011-1018-1

Xu G, Guo C, Shan H, Kong, H (2012). Divergence of duplicate genes in exon-intron structure. Proceedings of the National Academy of Sciences of the United States of America 109(4):1187-1192. https://doi.org/10.1073/pnas.1109047109

Ye JB, Cheng SY, Zhou X, Chen ZX, Kim SU, Tan JP, … Zhu YX (2019). A global survey of full-length transcriptome of Ginkgo biloba reveals transcript variants involved in flavonoid biosynthesis. Industrial Crops and Products 139:111547. https://doi.org/10.1016/j.indcrop.2019.111547

Zou XD, Hu XJ, Ma J, Li T, Ye ZQ, Wu YD (2016). Genome-wide analysis of WD40 protein family in human. Scientific Reports 6:39262. https://doi.org/10.1038/srep39262

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Published

2021-06-18

How to Cite

ZHENG, J. ., LIAO, Y. ., XU, F. ., ZHOU, X. ., YE, J. ., FU, M. ., LIU, X. ., CAO, Z. ., & ZHANG, W. . (2021). Genome-wide identification of WD40 superfamily genes and prediction of WD40 gene of flavonoid-related genes in Ginkgo biloba. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(2), 12086. https://doi.org/10.15835/nbha49212086

Issue

Vol. 49 No. 2 (2021)

Section

Research Articles
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DOI: 10.15835/nbha49212086

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Copyright (c) 2021 Jiarui ZHENG, Yongling LIAO, Feng XU, Xian ZHOU, Jiabao YE, Mingyue FU, Xiaomeng LIU, Zhengyan CAO, Weiwei ZHANG

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