Skip to main content
SpringerLink
Log in

Genome-wide analysis and transcriptional reprogrammings of MYB superfamily revealed positive insights into abiotic stress responses and anthocyanin accumulation in Carthamus tinctorius L.

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The MYB transcription factors comprise one of the largest superfamilies in plants that have been implicated in the regulation of plant-specific metabolites and responses to biotic and abiotic stresses. Here, we present the first comprehensive genome-wide analysis and functional characterization of the CtMYB family in Carthamus tinctorius. A total of 272 CtMYBs were identified and classified into 12 subgroups using comparative phylogenetic analysis with Arabidopsis and rice orthologs. The overview of conserved motifs, gene structures, and cis elements as well as the expression pattern of CtMYB genes indicated the diverse roles of these transcription factors during plant growth, regulation of secondary metabolites, and various abiotic stress responses. The subcellular localization and transactivation analysis of four CtMYB proteins indicated predominant localization in the nuclei with enhanced transcriptional activation in yeast. The expression of CtMYB63 induced with various abiotic stress conditions showed upregulation in its transcription level. In addition, the expression analysis of the core structural genes of anthocyanin biosynthetic pathway under drought and cold stress in CtMYB63 overexpressed transgenic lines also supports the notion of CtMYB63 transcriptional reprogramming in response to abiotic stress by upregulating the anthocyanin biosynthesis. Together, our findings revealed the underlying regulatory mechanism of CtMYB TF network involving enhanced cold and drought stress tolerance through activating the rapid biosynthesis of anthocyanin in C. tinctorius. This study also presents useful insights towards the establishment of new strategies for crop improvements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The draft genome sequence of C. tinctorius available at the NCBI (https://www.ncbi.nlm.nih.gov) under accession number (PRJNA399628; submitted on august 23rd, 2017).

References

  • Ahmad N, Jianyu L, Xu T, Noman M, Jameel A, Na Y, Yuanyuan D, Nan W, Xiaowei L, Fawei W et al (2019) Overexpression of a novel cytochrome P450 promotes flavonoid biosynthesis and osmotic stress tolerance in transgenic arabidopsis. Genes (basel) 10:756

    CAS  Google Scholar 

  • Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13:99–102

    CAS  PubMed  Google Scholar 

  • An JP, Li R, Qu FJ, You CX, Wang XF, Hao YJ (2018) R2R3-MYB transcription factor MdMYB23 is involved in the cold tolerance and proanthocyanidin accumulation in apple. Plant J 96:562–577

    CAS  PubMed  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202-208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Niu X, Guan Y, Li H (2017) Genome-wide analysis and expression profiles of the MYB genes in brachypodium distachyon. Plant Cell Physiol 58:1777–1788

    CAS  PubMed  Google Scholar 

  • Chujo T, Miyamoto K, Shimogawa T, Shimizu T, Otake Y, Yokotani N, Nishizawa Y, Shibuya N, Nojiri H, Yamane H et al (2013) OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol Biol 82:23–37

    CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x

    Article  CAS  PubMed  Google Scholar 

  • Du H, Yang SS, Liang Z, Feng BR, Liu L, Huang YB, Tang YX (2012) Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol 12:106

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duan F, Ding J, Lee D, Lu X, Feng Y, Song W (2017) Overexpression of SoCYP85A1, a spinach cytochrome p450 gene in transgenic tobacco enhances root development and drought stress tolerance. Front Plant Sci 8:1909

    PubMed  PubMed Central  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

    CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    CAS  PubMed  Google Scholar 

  • Fedoroff N (2001) How jumping genes were discovered. Nat Struct Biol 8:300–301

    CAS  PubMed  Google Scholar 

  • Gao J, Zhang Y, Zhang C, Qi F, Li X, Mu S, Peng Z (2014) Characterization of the floral transcriptome of moso bamboo (Phyllostachys edulis) at different flowering developmental stages by transcriptome sequencing and RNA-seq analysis. PLoS ONE 9:e98910

    PubMed  PubMed Central  Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez A, Mendenhall J, Huo Y, Lloyd A (2009) TTG1 complex MYBs, MYB5 and TT2, control outer seed coat differentiation. Dev Biol 325:412–421

    CAS  PubMed  Google Scholar 

  • Guo ZJ, Chen XJ, Wu XL, Ling JQ, Xu P (2004) Overexpression of the AP2/EREBP transcription factor OPBP1 enhances disease resistance and salt tolerance in tobacco. Plant Mol Biol 55:607–618

    CAS  PubMed  Google Scholar 

  • Hernández I, Alegre L, Van Breusegem F, Munné-Bosch S (2009) How relevant are flavonoids as antioxidants in plants? Trends Plant Sci 14:125–132

    PubMed  Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585-587

    PubMed  PubMed Central  Google Scholar 

  • Hsu CC, Chen YY, Tsai WC, Chen WH, Chen HH (2015) Three R2R3-MYB transcription factors regulate distinct floral pigmentation patterning in phalaenopsis spp. Plant Physiol 168:175–191

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    PubMed  PubMed Central  Google Scholar 

  • Huang C, Hu G, Li F, Li Y, Wu J, Zhou X (2013) NbPHAN, a MYB transcriptional factor, regulates leaf development and affects drought tolerance in nicotiana benthamiana. Physiol Plant 149:297–309

    CAS  PubMed  Google Scholar 

  • Huang CK, Lo PC, Huang LF, Wu SJ, Yeh CH, Lu CA (2015) A single-repeat MYB transcription repressor, MYBH, participates in regulation of leaf senescence in Arabidopsis. Plant Mol Biol 88:269–286

    CAS  PubMed  Google Scholar 

  • Huang Y, Zhao H, Gao F, Yao P, Deng R, Li C, Chen H, Wu Q (2018) A R2R3-MYB transcription factor gene, FtMYB13, from Tartary buckwheat improves salt/drought tolerance in Arabidopsis. Plant Physiol Biochem 132:238–248

    CAS  PubMed  Google Scholar 

  • Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci 18:477–483

    CAS  PubMed  Google Scholar 

  • Jailani AAK, Kumar A, Mandal B, Sivasudha T, Roy A (2016) Agroinfection of tobacco by croton yellow vein mosaic virus and designing of a replicon vector for expression of foreign gene in plant. Virusdisease 27:277–286

    PubMed  PubMed Central  Google Scholar 

  • Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41:577–585

    CAS  PubMed  Google Scholar 

  • Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045

    CAS  PubMed  Google Scholar 

  • Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN (2005) MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17:2981–2992

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal KC (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genom 13:544

    CAS  Google Scholar 

  • Kirik V, Lee MM, Wester K, Herrmann U, Zheng Z, Oppenheimer D, Schiefelbein J, Hulskamp M (2005) Functional diversification of MYB23 and GL1 genes in trichome morphogenesis and initiation. Development 132:1477–1485

    CAS  PubMed  Google Scholar 

  • Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C et al (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16:263–276

    CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    CAS  PubMed  Google Scholar 

  • Lee WJ, Jeong CY, Kwon J, Van Kien V, Lee D, Hong SW, Lee H (2016) Drastic anthocyanin increase in response to PAP1 overexpression in fls1 knockout mutant confers enhanced osmotic stress tolerance in Arabidopsis thaliana. Plant Cell Rep 35:2369–2379

    CAS  PubMed  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    CAS  PubMed  Google Scholar 

  • Li SF, Milliken ON, Pham H, Seyit R, Napoli R, Preston J, Koltunow AM, Parish RW (2009) The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed coat development, and trichome morphogenesis. Plant Cell 21:72–89

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Peng R, Tian Y, Han H, Xu J, Yao Q (2016) Genome-Wide Identification and Analysis of the MYB Transcription Factor Superfamily in Solanum lycopersicum. Plant Cell Physiol 57:1657–1677

    CAS  PubMed  Google Scholar 

  • Li WF, Mao J, Yang SJ, Guo ZG, Ma ZH, Dawuda MM, Zuo CW, Chu MY, Chen BH (2018) Anthocyanin accumulation correlates with hormones in the fruit skin of “Red Delicious” and its four generation bud sport mutants. BMC Plant Biol 18:363

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin-Wang K, McGhie TK, Wang M, Liu Y, Warren B, Storey R, Espley RV, Allan AC (2014) Engineering the anthocyanin regulatory complex of strawberry (Fragaria vesca). Front Plant Sci 5:651

    PubMed  PubMed Central  Google Scholar 

  • Lipsick JS (1996) One billion years of Myb. Oncogene 13:223–235

    CAS  PubMed  Google Scholar 

  • Liu X, Dong Y, Yao N, Zhang Y, Wang N, Cui X, Li X, Wang Y, Wang F, Yang J et al (2015) De novo sequencing and analysis of the safflower transcriptome to discover putative genes associated with safflor yellow in carthamus tinctorius L. Int J Mol Sci 16:25657–25677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Ahmad N, Yang L, Fu T, Kong J, Yao N, Dong Y, Wang N, Li X, Wang F et al (2019) Molecular cloning and functional characterization of chalcone isomerase from Carthamus tinctorius. AMB Express 9:132

    PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551–2565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mondal SK, Roy S (2018) Genome-wide sequential, evolutionary, organizational and expression analyses of phenylpropanoid biosynthesis associated MYB domain transcription factors in Arabidopsis. J Biomol Struct Dyn 36:1577–1601

    CAS  PubMed  Google Scholar 

  • Nakabayashi R, Yonekura-Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T, Matsuda F, Kojima M, Sakakibara H, Shinozaki K et al (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77:367–379

    CAS  PubMed  Google Scholar 

  • Nakata M, Mitsuda N, Herde M, Koo AJ, Moreno JE, Suzuki K, Howe GA, Ohme-Takagi M (2013) A bHLH-type transcription factor, ABA-inducible BHLH-type transcription factor/JA-associated MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in arabidopsis. Plant Cell 25:1641–1656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H (1987a) The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. Embo J 6:3553–3558

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Z, Lu Y, Li L, Zhao Q, Feng Q, Gao Z, Lu H, Hu T, Yao N, Liu K et al (2013) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla). Nat Genet 45:456–461

    CAS  PubMed  Google Scholar 

  • Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant J 40:979–995

    CAS  PubMed  Google Scholar 

  • Ptashne M (1988) How eukaryotic transcriptional activators work. Nature 335:683–689

    CAS  PubMed  Google Scholar 

  • Reeves PH, Ellis CM, Ploense SE, Wu MF, Yadav V, Tholl D, Chételat A, Haupt I, Kennerley BJ, Hodgens C et al (2012) A regulatory network for coordinated flower maturation. PLoS Genet 8:e1002506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-Z, Keddie J, Adam L, Pineda O, Ratcliffe O, Samaha R (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    CAS  PubMed  Google Scholar 

  • Roh JS, Han JY, Kim JH, Hwang JK (2004) Inhibitory effects of active compounds isolated from safflower (Carthamus tinctorius L.) seeds for melanogenesis. Biol Pharm Bull 27:1976–1978

    CAS  PubMed  Google Scholar 

  • Romero I, Fuertes A, Benito MJ, Malpica JM, Leyva A, Paz-Ares J (1998) More than 80R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J 14:273–284

    CAS  PubMed  Google Scholar 

  • Ronchi A, Petroni K, Tonelli C (1995) The reduced expression of endogenous duplications (REED) in the maize R gene family is mediated by DNA methylation. EMBO J 14:5318–5328

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosinski JA, Atchley WR (1998) Molecular evolution of the Myb family of transcription factors: evidence for polyphyletic origin. J Mol Evol 46:74–83

    CAS  PubMed  Google Scholar 

  • Saha G, Park JI, Ahmed NU, Kayum MA, Kang KK, Nou IS (2016) Characterization and expression profiling of MYB transcription factors against stresses and during male organ development in Chinese cabbage (Brassica rapa ssp. pekinensis). Plant Physiol Biochem 104:200–215

    CAS  PubMed  Google Scholar 

  • Salih H, Gong W, He S, Sun G, Sun J, Du X (2016) Genome-wide characterization and expression analysis of MYB transcription factors in Gossypium hirsutum. BMC Genet 17:129

    PubMed  PubMed Central  Google Scholar 

  • Schaart JG, Dubos C, Romero De La Fuente I, van Houwelingen AM, de Vos RC, Jonker HH, Xu W, Routaboul JM, Lepiniec L, Bovy AG (2013) Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria × ananassa) fruits. New Phytol 197:454–467

    CAS  PubMed  Google Scholar 

  • Schwinn K, Venail J, Shang Y, Mackay S, Alm V, Butelli E, Oyama R, Bailey P, Davies K, Martin C (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18:831–851

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol 151:275–289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shen X, Guo X, Guo X, Zhao D, Zhao W, Chen J, Li T (2017) PacMYBA, a sweet cherry R2R3-MYB transcription factor, is a positive regulator of salt stress tolerance and pathogen resistance. Plant Physiol Biochem 112:302–311

    CAS  PubMed  Google Scholar 

  • Shi SG, Yang M, Zhang M, Wang P, Kang YX, Liu JJ (2014) Genome-wide transcriptome analysis of genes involved in flavonoid biosynthesis between red and white strains of Magnolia sprengeri pamp. BMC Genomics 15:706

    PubMed  PubMed Central  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Urao T, Koizumi M (1992) Nucleotide sequence of a gene from Arabidopsis thaliana encoding a myb homologue. Plant Mol Biol 19:493–499

    CAS  PubMed  Google Scholar 

  • Smita S, Katiyar A, Chinnusamy V, Pandey DM, Bansal KC (2015) Transcriptional regulatory network analysis of MYB transcription factor family genes in rice. Front Plant Sci 6:1157

    PubMed  PubMed Central  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001a) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    CAS  PubMed  Google Scholar 

  • Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660–677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thao NT, Cuong TD, Hung TM, Lee JH, Na M, Son JK, Jung HJ, Fang Z, Woo MH, Choi JS et al (2011) Simultaneous determination of bioactive flavonoids in some selected Korean thistles by high-performance liquid chromatography. Arch Pharm Res 34:455–461

    PubMed  Google Scholar 

  • Tominaga-Wada R, Wada T (2014) Regulation of root hair cell differentiation by R3 MYB transcription factors in tomato and Arabidopsis. Front Plant Sci 5:91

    PubMed  PubMed Central  Google Scholar 

  • Vailleau F, Daniel X, Tronchet M, Montillet JL, Triantaphylidès C, Roby D (2002) A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc Natl Acad Sci USA 99:10179–10184

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Wang JW, Yu N, Li CH, Luo B, Gou JY, Wang LJ, Chen XY (2004) Control of plant trichome development by a cotton fiber MYB gene. Plant Cell 16:2323–2334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zhang X, Zhao Y, Yang J, He Y, Li G, Ma W, Huang X, Su J (2020) Transcription factor PyHY5 binds to the promoters of PyWD40 and PyMYB10 and regulates its expression in red pear “Yunhongli No. 1.” Plant Physiol Biochem 154:665–674

    CAS  PubMed  Google Scholar 

  • Wei H, Zhao H, Su T, Bausewein A, Greiner S, Harms K, Rausch T (2017) Chicory R2R3-MYB transcription factors CiMYB5 and CiMYB3 regulate fructan 1-exohydrolase expression in response to abiotic stress and hormonal cues. J Exp Bot 68:4323–4338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223

    CAS  PubMed  Google Scholar 

  • Wood LK, Thiele DJ (2009) Transcriptional activation in yeast in response to copper deficiency involves copper-zinc superoxide dismutase. J Biol Chem 284:404–413

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu C, Zhang J, Zhou T, Guo B, Wang Y, Hou J (2011) Simultaneous determination of seven flavonoids in dog plasma by ultra-performance liquid chromatography-tandem mass spectrometry and its application to a bioequivalence study of bioactive components in Herba Epimedii and Er-Xian decoction. J Pharm Biomed Anal 54:186–191

    CAS  PubMed  Google Scholar 

  • Xie Y, Chen P, Yan Y, Bao C, Li X, Wang L, Shen X, Li H, Liu X, Niu C et al (2018) An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple. New Phytol 218:201–218

    CAS  PubMed  Google Scholar 

  • Xu H, Yang G, Zhang J, Wang Y, Zhang T, Wang N, Jiang S, Zhang Z, Chen X (2018) Overexpression of a repressor MdMYB15L negatively regulates anthocyanin and cold tolerance in red-fleshed callus. Biochem Biophys Res Commun 500:405–410

    CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    CAS  PubMed  Google Scholar 

  • Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ye SY, Gao WY (2008) Hydroxysafflor yellow A protects neuron against hypoxia injury and suppresses inflammatory responses following focal ischemia reperfusion in rats. Arch Pharm Res 31:1010–1015

    CAS  PubMed  Google Scholar 

  • Ye H, Du H, Tang N, Li X, Xiong L (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71:291–305

    CAS  PubMed  Google Scholar 

  • Yingqi H, Ahmad N, Yuanyuan T, Jianyu L, Liyan W, Gang W, Xiuming L, Yuanyuan D, Fawei W, Weican L et al (2019) Genome-wide identification, expression analysis, and subcellular localization of carthamus tinctorius bHLH transcription factors. Int J Mol Sci 20:3044

    Google Scholar 

  • Zhang ZL, Shin M, Zou X, Huang J, Ho TH, Shen QJ (2009) A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells. Plant Mol Biol 70:139–151

    CAS  PubMed  Google Scholar 

  • Zhang Y, Guo J, Dong H, Zhao X, Zhou L, Li X, Liu J, Niu Y (2011) Hydroxysafflor yellow A protects against chronic carbon tetrachloride-induced liver fibrosis. Eur J Pharmacol 660:438–444

    CAS  PubMed  Google Scholar 

  • Zhang L, Dong C, Zhang Q, Zhao G, Li F, Xia C, Zhang L, Han L, Wu J, Jia J et al (2016) The wheat MYB transcription factor TaMYB18 regulates leaf rolling in rice. Biochem Biophys Res Commun 481:77–83

    CAS  PubMed  Google Scholar 

  • Zhao D, Tao J, Han C, Ge J (2012) Flower color diversity revealed by differential expression of flavonoid biosynthetic genes and flavonoid accumulation in herbaceous peony (Paeonia lactiflora Pall.). Mol Biol Rep 39:11263–11275

    CAS  PubMed  Google Scholar 

  • Zhou L, He Y, Li J, Liu Y, Chen H (2020) CBFs function in anthocyanin biosynthesis by interacting with MYB113 in eggplant (Solanum melongena L.). Plant Cell Physiol 61:416–426

    CAS  PubMed  Google Scholar 

  • Zhu L, Shan H, Chen S, Jiang J, Gu C, Zhou G, Chen Y, Song A, Chen F (2013) The heterologous expression of the chrysanthemum R2R3-MYB transcription factor CmMYB1 alters lignin composition and represses flavonoid synthesis in arabidopsis thaliana. PLoS ONE 8:e65680

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmermann IM, Heim MA, Weisshaar B, Uhrig JF (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40:22–34

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by grants from the National Natural Science Foundation of China (No. 31771868, 31501366), the Science and Technology Development Project of Jilin Province (No. 20190201172JC, 20190201175JC, 20150623024TC-11), Student innovation and entrepreneurship training program of Jilin Agricultural University.

Author information

Author notes

  1. Yingqi Hong and Naveed Ahmad have contributed equally to this work.

Authors and Affiliations

  1. Engineering Research Center of the Chinese Ministry of Education for Bioreactor and Pharmaceutical Development, College of Life Sciences, Jilin Agricultural University, Changchun, 130118, China

    Yingqi Hong, Naveed Ahmad, Jianyi Zhang, Yanxi Lv, Xinyue Zhang, Xintong Ma, Liu Xiuming & Yao Na

Authors
  1. Yingqi Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naveed Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianyi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanxi Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xinyue Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xintong Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Liu Xiuming
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yao Na
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LX and YN designed the project; H Y and NA performed the experiments and analyze the data; JZ, and YX carried out formal analysis; XY and XT performed statistical analysis; NA conducted software analysis, HY wrote the original draft.

Corresponding authors

Correspondence to Liu Xiuming or Yao Na.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Bing yang.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hong, Y., Ahmad, N., Zhang, J. et al. Genome-wide analysis and transcriptional reprogrammings of MYB superfamily revealed positive insights into abiotic stress responses and anthocyanin accumulation in Carthamus tinctorius L.. Mol Genet Genomics 297, 125–145 (2022). https://doi.org/10.1007/s00438-021-01839-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-021-01839-1

Keywords

Search

Navigation