Genome-wide identification and analysis of anthocyanin synthesis-related R2R3-MYB genes in Fragaria pentaphylla.
Fragaria pentaphylla
Anthocyanin biosynthesis
R2R3-MYB
Subcellular localization
Transcriptome
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
13 Oct 2024
13 Oct 2024
Historique:
received:
13
06
2024
accepted:
08
10
2024
medline:
14
10
2024
pubmed:
14
10
2024
entrez:
13
10
2024
Statut:
epublish
Résumé
MYB transcription factors regulate anthocyanin biosynthesis across numerous plant species. However, comprehensive genome-wide investigations regarding the R2R3-MYB gene family and its involvement in regulating anthocyanin biosynthesis in the red and white fruit color morphs of Fragaria pentaphylla remain scarce. A total of 101 FpR2R3-MYB genes were identified from the F. pentaphylla genome and were divided into 34 subgroups based on phylogenetic analysis. Gene structure (exon/intron) and protein motifs were particularly conserved among the FpR2R3-MYB genes, especially members within the same subgroup. The FpR2R3-MYB genes were distributed over seven F. pentaphylla chromosomes. Analysis of gene duplication events revealed five pairs of tandem duplication genes and 16 pairs of segmental duplication genes, suggesting that segmental duplications are the major pattern for expansion of the FpR2R3-MYB gene family expansion in F. pentaphylla. Cis-regulatory elements of the FpR2R3-MYB promoters were involved in cellular development, phytohormones, environmental stress and photoresponse. Based on the analysis of the FpR2R3-MYB gene family and transcriptome sequencing (RNA-seq) data, FpMYB9 was identified as a key transcription factor involved in the regulation of anthocyanin synthesis in F. pentaphylla fruits. The expression of FpMYB9 increases significantly during the ripening stage of red fruits, as confirmed by reverse transcription quantitative real-time PCR. In addition, subcellular localization experiments further confirmed the nuclear presence of FpMYB9, supporting its role as a transcription factor involved in anthocyanin biosynthesis. Our results showed that the FpR2R3-MYB genes are highly conserved and play important roles in the anthocyanin biosynthesis in F. pentaphylla fruits. Our results also provide a compelling basis for further understanding of the regulatory mechanism underlying the role of FpMYB9 in anthocyanin formation in F. pentaphylla fruits.
Sections du résumé
BACKGROUND
BACKGROUND
MYB transcription factors regulate anthocyanin biosynthesis across numerous plant species. However, comprehensive genome-wide investigations regarding the R2R3-MYB gene family and its involvement in regulating anthocyanin biosynthesis in the red and white fruit color morphs of Fragaria pentaphylla remain scarce.
RESULTS
RESULTS
A total of 101 FpR2R3-MYB genes were identified from the F. pentaphylla genome and were divided into 34 subgroups based on phylogenetic analysis. Gene structure (exon/intron) and protein motifs were particularly conserved among the FpR2R3-MYB genes, especially members within the same subgroup. The FpR2R3-MYB genes were distributed over seven F. pentaphylla chromosomes. Analysis of gene duplication events revealed five pairs of tandem duplication genes and 16 pairs of segmental duplication genes, suggesting that segmental duplications are the major pattern for expansion of the FpR2R3-MYB gene family expansion in F. pentaphylla. Cis-regulatory elements of the FpR2R3-MYB promoters were involved in cellular development, phytohormones, environmental stress and photoresponse. Based on the analysis of the FpR2R3-MYB gene family and transcriptome sequencing (RNA-seq) data, FpMYB9 was identified as a key transcription factor involved in the regulation of anthocyanin synthesis in F. pentaphylla fruits. The expression of FpMYB9 increases significantly during the ripening stage of red fruits, as confirmed by reverse transcription quantitative real-time PCR. In addition, subcellular localization experiments further confirmed the nuclear presence of FpMYB9, supporting its role as a transcription factor involved in anthocyanin biosynthesis.
CONCLUSION
CONCLUSIONS
Our results showed that the FpR2R3-MYB genes are highly conserved and play important roles in the anthocyanin biosynthesis in F. pentaphylla fruits. Our results also provide a compelling basis for further understanding of the regulatory mechanism underlying the role of FpMYB9 in anthocyanin formation in F. pentaphylla fruits.
Identifiants
pubmed: 39396954
doi: 10.1186/s12864-024-10882-2
pii: 10.1186/s12864-024-10882-2
doi:
Substances chimiques
Anthocyanins
0
Transcription Factors
0
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
952Subventions
Organisme : National Natural Science Foundation of China
ID : 31261120580
Informations de copyright
© 2024. The Author(s).
Références
Jezek M, Zorb C, Merkt N, Geilfus CM. Anthocyanin management in fruits by fertilization. J Agric Food Chem. 2018;66(4):753–64.
pubmed: 29297687
doi: 10.1021/acs.jafc.7b03813
Garcia-Alonso M, Rimbach G, Sasai M, Nakahara M, Matsugo S, Uchida Y, Rivas-Gonzalo JC, De Pascual-Teresa S. Electron spin resonance spectroscopy studies on the free radical scavenging activity of wine anthocyanins and pyranoanthocyanins. Mol Nutr Food Res. 2005;49(12):1112–9.
pubmed: 16254886
doi: 10.1002/mnfr.200500100
Garcia-Alonso M, Rimbach G, Rivas-Gonzalo JC, De Pascual-Teresa S. Antioxidant and cellular activities of anthocyanins and their corresponding vitisins A–studies in platelets, monocytes, and human endothelial cells. J Agric Food Chem. 2004;52(11):3378–84.
pubmed: 15161201
doi: 10.1021/jf035360v
Kamei H, Hashimoto Y, Koide T, Kojima T, Hasegawa M. Anti-tumor effect of methanol extracts from red and white wines. Cancer Biother Radio. 1998;13(6):447–52.
Fimognari C, Berti F, Nusse M, Cantelli-Forti G, Hrelia P. Induction of apoptosis in two human leukemia cell lines as well as differentiation in human promyelocytic cells by cyanidin-3-o-beta-glucopyranoside. Biochem Pharmacol. 2004;67(11):2047–56.
pubmed: 15135302
doi: 10.1016/j.bcp.2004.02.021
Kong JM, Chia LS, Goh NK, Chia TF, Brouillard R. Analysis and biological activities of anthocyanins. Phytochemistry. 2003;64(5):923–33.
pubmed: 14561507
doi: 10.1016/S0031-9422(03)00438-2
Li J, Wu K, Li L, Ma G, Fang L, Zeng S. Transcriptomic analysis reveals biosynthesis genes and transcription factors related to leaf anthocyanin biosynthesis in Aglaonema commutatum. BMC Genomics. 2023;24(1):28.
pubmed: 36650457
pmcid: 9847206
doi: 10.1186/s12864-022-09107-1
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci. 2010;15(10):573–81.
pubmed: 20674465
doi: 10.1016/j.tplants.2010.06.005
Wang X, Niu Y, Zheng Y. Multiple functions of MYB transcription factors in abiotic stress responses. Int J Mol Sci 2021;22(11):6125.
Li C, Yu W, Xu J, Lu X, Liu Y. Anthocyanin biosynthesis induced by MYB transcription factors in plants. Int J Mol Sci. 2022;23(19):11701.
Prouse MB, Campbell MM. The interaction between MYB proteins and their target DNA binding sites. Biochim Biophys Acta. 2012;1819(1):67–77.
pubmed: 22067744
doi: 10.1016/j.bbagrm.2011.10.010
Ogata K, Kanei-Ishii C, Sasaki M, Hatanaka H, Nagadoi A, Enari M, Nakamura H, Nishimura Y, Ishii S, Sarai A. The cavity in the hydrophobic core of myb DNA-binding domain is reserved for DNA recognition and trans-activation. Nat Struct Biol. 1996;3(2):178–87.
pubmed: 8564545
doi: 10.1038/nsb0296-178
Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal KC. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics. 2012;13:544.
pubmed: 23050870
pmcid: 3542171
doi: 10.1186/1471-2164-13-544
Yan H, Pei X, Zhang H, Li X, Zhang X, Zhao M, Chiang VL, Sederoff RR, Zhao X. MYB-mediated regulation of anthocyanin biosynthesis. Int J Mol Sci. 2021;22(6):3103.
Zhao M, Li J, Zhu L, Chang P, Li L, Zhang L. Identification and characterization of MYB-bHLH-WD40 regulatory complex members controlling anthocyanidin biosynthesis in blueberry fruits development. Genes-Basel. 2019;10(7):496.
Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodriguez-Franco A, Caballero JL, Schwab W, Munoz-Blanco J, Blanco-Portales R. MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria x ananassa fruits. J EXP BOT. 2014;65(2):401–17.
pubmed: 24277278
doi: 10.1093/jxb/ert377
Aharoni A, De Vos CH, Wein M, Sun Z, Greco R, Kroon A, Mol JN, O’Connell AP. The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. PLANT J. 2001;28(3):319–32.
pubmed: 11722774
doi: 10.1046/j.1365-313X.2001.01154.x
Martinez-Rivas FJ, Blanco-Portales R, Serratosa MP, Ric-Varas P, Guerrero-Sanchez V, Medina-Puche L, Moyano L, Mercado JA, Alseekh S, Caballero JL, et al. FaMYB123 interacts with FabHLH3 to regulate the late steps of anthocyanin and flavonol biosynthesis during ripening. PLANT J. 2023;114(3):683–98.
pubmed: 36840368
doi: 10.1111/tpj.16166
Luo X, Plunkert M, Teng Z, Mackenzie K, Guo L, Luo Y, Hytonen T, Liu Z. Two MYB activators of anthocyanin biosynthesis exhibit specialized activities in petiole and fruit of diploid strawberry. J EXP BOT. 2023;74(5):1517–31.
pubmed: 36546359
doi: 10.1093/jxb/erac507
Li L, Ban ZJ, Li XH, Wu MY, Wang AL, Jiang YQ, Jiang YH. Differential expression of anthocyanin biosynthetic genes and transcription factor PcMYB10 in pears (Pyrus communis L). PLoS ONE. 2012;7(9):e46070.
pubmed: 23029391
pmcid: 3460990
doi: 10.1371/journal.pone.0046070
Ravaglia D, Espley RV, Henry-Kirk RA, Andreotti C, Ziosi V, Hellens RP, Costa G, Allan AC. Transcriptional regulation of flavonoid biosynthesis in nectarine (Prunus persica) by a set of R2R3 MYB transcription factors. BMC Plant Biol. 2013;13:68.
pubmed: 23617716
pmcid: 3648406
doi: 10.1186/1471-2229-13-68
Jin W, Wang H, Li M, Wang J, Yang Y, Zhang X, Yan G, Zhang H, Liu J, Zhang K. The R2R3 MYB transcription factor PavMYB10.1 involves in anthocyanin biosynthesis and determines fruit skin colour in sweet cherry (Prunus avium L). Plant Biotechnol J. 2016;14(11):2120–33.
pubmed: 27107393
pmcid: 5095807
doi: 10.1111/pbi.12568
Xi W, Feng J, Liu Y, Zhang S, Zhao G. The R2R3-MYB transcription factor PaMYB10 is involved in anthocyanin biosynthesis in apricots and determines red blushed skin. BMC Plant Biol. 2019;19(1):287.
pubmed: 31262258
pmcid: 6604168
doi: 10.1186/s12870-019-1898-4
Shen J, Shao W, Li J, Lu H. Integrated metabolomic and transcriptomic analysis reveals factors underlying differences in fruit quality between Fragaria Nilgerrensis and Fragaria pentaphylla. J Sci Food Agr. 2022;102(8):3287–96.
doi: 10.1002/jsfa.11674
Liu J, Wang J, Wang M, Zhao J, Zheng Y, Zhang T, Xue L, Lei J. Genome-wide analysis of the R2R3-MYB Gene Family in Fragaria × ananassa and its function identification during anthocyanins Biosynthesis in Pink-flowered Strawberry. Front Plant Sci. 2021;12:702160.
pubmed: 34527006
pmcid: 8435842
doi: 10.3389/fpls.2021.702160
Wang J, Yin Y, Gao H, Sheng L. Identification of MYB transcription factors involving in fruit quality regulation of Fragaria × Ananassa Duch. Genes-Basel 2022;14(1):68.
Bai L, Chen Q, Jiang L, Lin Y, Ye Y, Liu P, Wang X, Tang H. Comparative transcriptome analysis uncovers the regulatory functions of long noncoding RNAs in fruit development and color changes of Fragaria pentaphylla. Hortic Res. 2019;6:42.
Duan W, Sun P, Li J. Expression of genes involved in the anthocyanin biosynthesis pathway in white and red fruits of Fragaria pentaphylla and genetic variation in the dihydroflavonol-4-reductase gene. Biochem Syst Ecol. 2017;72:40–6.
Lin H, Chen L, Cai C, Ma J, Li J, Ashman T, Liston A, Dong M. Genomic data provides insights into the evolutionary history and adaptive differentiation of two tetraploid strawberries. Hortic Res-England. 2024;326:112751.
Garcia-Hernandez M, Berardini TZ, Chen G, Crist D, Doyle A, Huala E, Knee E, Lambrecht M, Miller N, Mueller LA, et al. TAIR: a resource for integrated Arabidopsis data. Funct Integr Genomic. 2002;2(6):239–53.
doi: 10.1007/s10142-002-0077-z
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42(Database issue):D222–30.
pubmed: 24288371
doi: 10.1093/nar/gkt1223
Letunic I, Khedkar S, Bork P. SMART: recent updates, new developments and status in 2020. Nucleic Acids Res. 2021;49(D1):D458–60.
pubmed: 33104802
doi: 10.1093/nar/gkaa937
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol. 1999;112:531–52.
pubmed: 10027275
Fan P, Lin QH, Guo Y, Zhao LL, Ning H, Liu MY, Wei DQ. The PPI network analysis of mRNA expression profile of uterus from primary dysmenorrheal rats. Sci Rep. 2018;8(1):351.
pubmed: 29321498
pmcid: 5762641
doi: 10.1038/s41598-017-18748-2
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–504.
pubmed: 14597658
pmcid: 403769
doi: 10.1101/gr.1239303
Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40(7):e49.
pubmed: 22217600
pmcid: 3326336
doi: 10.1093/nar/gkr1293
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40(Database issue):D1178–86.
pubmed: 22110026
doi: 10.1093/nar/gkr944
Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, Cui X, Peng L. Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. Bmc Plant Biol. 2010;10:282.
pubmed: 21167079
pmcid: 3022907
doi: 10.1186/1471-2229-10-282
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–8. (Web Server issue).
pubmed: 19458158
pmcid: 2703892
doi: 10.1093/nar/gkp335
Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188–90.
pubmed: 15173120
pmcid: 419797
doi: 10.1101/gr.849004
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947–8.
pubmed: 17846036
doi: 10.1093/bioinformatics/btm404
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9.
pubmed: 29722887
pmcid: 5967553
doi: 10.1093/molbev/msy096
Stracke R, Werber M, Weisshaar B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol. 2001;4(5):447–56.
pubmed: 11597504
doi: 10.1016/S1369-5266(00)00199-0
Jin Y, Liu B, Li C, Shi S. Origin identification of Cornus officinalis based on PCA-SVM combined model. PLoS ONE. 2023;18(2):e282429.
doi: 10.1371/journal.pone.0282429
Tao Y, Chen L, Jin J, Du Z, Li J. Genome-wide identification and analysis of bZIP gene family reveal their roles during development and drought stress in wheel wingnut (Cyclocarya paliurus). BMC Genomics. 2022;23(1):743.
Yu CS, Lin CJ, Hwang JK. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci. 2004;13(5):1402–6.
pubmed: 15096640
pmcid: 2286765
doi: 10.1110/ps.03479604
Sparkes IA, Runions J, Kearns A, Hawes C. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc. 2006;1(4):2019–25.
pubmed: 17487191
doi: 10.1038/nprot.2006.286
Duan W, Shao W, Lin W, Yuan L, Lu Q, Chen L, Zagorchev L, Li J. Integrated metabolomics and transcriptomics reveal the differences in fruit quality of the red and white Fragaria pentaphylla morphs. Food Biosci. 2021;40:100896.
Hurst LD. The Ka/Ks ratio: diagnosing the form of sequence evolution. TRENDS GENET. 2002;18(9):486.
pubmed: 12175810
doi: 10.1016/S0168-9525(02)02722-1
Komatsuzaki A, Hoshino A, Otagaki S, Matsumoto S, Shiratake K. Genome-wide analysis of R2R3-MYB transcription factors in Japanese morning glory. PLoS ONE. 2022;17(10):e271012.
doi: 10.1371/journal.pone.0271012
Yang J, Zhang B, Gu G, Yuan J, Shen S, Jin L, Lin Z, Lin J, Xie X. Genome-wide identification and expression analysis of the R2R3-MYB gene family in tobacco (Nicotiana tabacum L). BMC Genomics. 2022;23(1):432.
pubmed: 35681121
pmcid: 9178890
doi: 10.1186/s12864-022-08658-7
Zhao P, Li Q, Li J, Wang L, Ren Z. Genome-wide identification and characterization of R2R3MYB family in Solanum lycopersicum. Mol Genet Genomics. 2014;289(6):1183–207.
pubmed: 25005853
doi: 10.1007/s00438-014-0879-4
Pu Z, Wei G, Liu Z, Chen L, Guo H, Li Y, Li Y, Dai S, Wang J, Li W, et al. Selenium and anthocyanins share the same transcription factors R2R3MYB and bHLH in wheat. FOOD CHEM. 2021;356:129699.
pubmed: 33873144
doi: 10.1016/j.foodchem.2021.129699
Du J, Zhang Q, Hou S, Chen J, Meng J, Wang C, Liang D, Wu R, Guo Y. Genome-wide identification and analysis of the R2R3-MYB gene family in Theobroma cacao. Genes-Basel. 2022;13(9):1572.
Naik J, Rajput R, Pucker B, Stracke R, Pandey A. The R2R3-MYB transcription factor MtMYB134 orchestrates flavonol biosynthesis in Medicago truncatula. Plant Mol Biol. 2021;106(1–2):157–72.
pubmed: 33704646
doi: 10.1007/s11103-021-01135-x
Wu Y, Wen J, Xia Y, Zhang L, Du H. Evolution and functional diversification of R2R3-MYB transcription factors in plants. Hortic Res. 2022;9:uhac58.
doi: 10.1093/hr/uhac058
Zhao L, Gao L, Wang H, Chen X, Wang Y, Yang H, Wei C, Wan X, Xia T. The R2R3-MYB, bHLH, WD40, and related transcription factors in flavonoid biosynthesis. Funct Integr Genomic. 2013;13(1):75–98.
doi: 10.1007/s10142-012-0301-4
Liu Y, Zhu L, Yang M, Xie X, Sun P, Fang C, Zhao J. R2R3-MYB transcription factor FaMYB5 is involved in citric acid metabolism in strawberry fruits. J Plant Physiol. 2022;277:153789.
pubmed: 35995002
doi: 10.1016/j.jplph.2022.153789
Matsui K, Oshima Y, Mitsuda N, Sakamoto S, Nishiba Y, Walker AR, Ohme-Takagi M, Robinson SP, Yasui Y, Mori M, et al. Buckwheat R2R3 MYB transcription factor FeMYBF1 regulates flavonol biosynthesis. Plant Sci. 2018;274:466–75.
pubmed: 30080636
doi: 10.1016/j.plantsci.2018.06.025
Kang YH, Kirik V, Hulskamp M, Nam KH, Hagely K, Lee MM, Schiefelbein J. The MYB23 gene provides a positive feedback loop for cell fate specification in the Arabidopsis root epidermis. Plant Cell. 2009;21(4):1080–94.
pubmed: 19395683
pmcid: 2685616
doi: 10.1105/tpc.108.063180
Tominaga-Wada R, Nukumizu Y, Sato S, Kato T, Tabata S, Wada T. Functional divergence of MYB-related genes, WEREWOLF and AtMYB23 in Arabidopsis. Biosci Biotech Biochem. 2012;76(5):883–7.
doi: 10.1271/bbb.110811
Lau SE, Schwarzacher T, Othman RY, Harikrishna JA. dsRNA silencing of an R2R3-MYB transcription factor affects flower cell shape in a Dendrobium hybrid. BMC Plant Biol. 2015;15:194.
Liu X, Yin X, Allan AC, Lin-Wang K, Shi Y, Huang Y, Ferguson IB, Xu C, Chen K. The role of MrbHLH1 and MrMYB1 in regulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis. Plant Cell Tissue Organ Cult (PCTOC). 2013;115(3):285–98.
doi: 10.1007/s11240-013-0361-8
Leng L, Zhang X, Liu W, Wu Z. Genome-wide identification of the MYB and bHLH families in carnations and expression analysis at different floral development stages. Int J Mol Sci 2023;24(11):9499.
Chen L, Cui Y, Yao Y, An L, Bai Y, Li X, Yao X, Wu K. Genome-wide identification of WD40 transcription factors and their regulation of the MYB-bHLH-WD40 (MBW) complex related to anthocyanin synthesis in Qingke (Hordeum vulgare L. var. nudum hook. F). BMC Genomics. 2023;24(1):166.