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Identification and expression analysis under abiotic stress of the R2R3-MYB genes in Ginkgo biloba L.

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Abstract

The R2R3-MYB gene family is the largest MYB subfamily in plants and is involved in the regulation of plant secondary metabolism and specific morphogenesis, as well as the response to biotic and abiotic stress. However, a systematic identification and characterization of this gene family has not been carried out in Ginkgo biloba. In this study, we performed a transcriptome-wide survey from four tissues of G. biloba to determine the genetic variation and expression pattern of the R2R3-MYB genes. We analyzed 45 GbMYBs and identified 42 with a complete coding sequence via conserved motif searches. The MYB domain and other motifs in GbMYBs are highly conserved with Arabidopsis thaliana AtMYBs. Phylogenetic analysis of the GbMYBs and AtMYBs categorized the R2R3-MYBs into 26 subgroups, of which 11 subgroups included proteins from both G. biloba and Arabidopsis, and 1 subgroup was specific to G. biloba. Moreover, the GbMYBs expression patterns were analyzed in different tissues and abiotic stress conditions. The results revealed that GbMYBs were differentially expressed in various tissues and following abiotic stresses and phytohormone treatments, indicating their possible roles in biological processes and abiotic stress tolerance and adaptation. Our study demonstrated the functional diversity of the GbMYBs and will provide a foundation for future research into their biological and molecular functions.

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References

  • Agarwal M, Hao Y, Kapoor A, Dong C, Fujii H, Zheng X, Zhu J (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645

    Article  CAS  PubMed  Google Scholar 

  • Allen RS, Li J, Stahle MI, Dubroué A, Gubler F, Millar AA (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci 104:16371–16376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Ann N Y Acad Sci 19:307–321

    CAS  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(Web Server issue):W202–W208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin H, Koes R, Roberts K, Martin C (2007) Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134:1691–1701

    Article  CAS  PubMed  Google Scholar 

  • Bedon F, Schiefelbein J, Pang M (2014) Members of the MYBMIXTA-like transcription factors may orchestrate the initiation of fiber development in cotton seeds. Front Plant Sci 5:72–75

    Article  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao Z, Zhang S, Wang R, Zhang R, Hao Y (2013) Genome wide analysis of the apple MYB transcription factor family allows the identification of MdoMYB121 gene confering abiotic stress tolerance in plants. PLoS ONE 8:e69955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Yang X, He K, Liu M, Li J, Gao Z, Lin Z, Zhang Y, Wang X, Qiu X, Shen Y, Zhang L, Deng X, Luo J, Deng X, Chen Z, Gu H, Qu L (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124

    Article  CAS  Google Scholar 

  • Cheng H, Li L, Cheng S, Cao F, Wang Y, Yuan H (2011) Molecular cloning and function assay of a chalcone isomerase gene (GbCHI) from Ginkgo biloba. Plant Cell Rep 30:49–62

    Article  CAS  PubMed  Google Scholar 

  • Cheng H, Li L, Xu F, Cheng S, Cao F, Wang Y, Yuan H, Jiang D, Wu C (2013) Expression patterns of a cinnamyl alcohol dehydrogenase gene involved in lignin biosynthesis and environmental stress in Ginkgo biloba. Plant Mol Biol 40:707–721

    CAS  Google Scholar 

  • Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C (2008) Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. Plant J 53:53–64

    Article  CAS  PubMed  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • DeFeudis FV, Drieu K (2000) Ginkgo biloba extract (EGb 761) and CNS functions basic studies and clinical applications. Curr Drug Targets 1:25–58

    Article  CAS  PubMed  Google Scholar 

  • DeFeudis FV, Papadopoulos V, Drieu K (2003) Ginkgo biloba extracts and cancer: a research area in its infancy. Fundam Clin Pharmacol 17:405–417

    Article  CAS  PubMed  Google Scholar 

  • Denekamp M, Smeekens SC (2003) Integration of wounding and osmotic stress signals determines the expression of the AtMYB102 transcription factor gene. Plant Physiol 132:1415–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Z, Li S, An X, Liu X, Qin H, Wang D (2009) Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genomics 36:17–29

    Article  CAS  PubMed  Google Scholar 

  • Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316–323

    Article  CAS  PubMed  Google Scholar 

  • Du H, Feng B, Yang S, Huang Y, Tang Y (2012) The R2R3-MYB transcription factor gene family in maize. PLoS ONE 7:1799–1823

    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

    Article  CAS  PubMed  Google Scholar 

  • 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 J 49:414–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564

    Article  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Gocal GF, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish RW, Dennis ES, Weigel D (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127:1682–1693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong Y, Liao Z, Guo B, Sun X, Tang K (2006) Molecular cloning and expression profile analysis of Ginkgo biloba DXS gene encoding 1-deoxy-D-xylulose 5-phosphate synthase, the first committed enzyme of the 2-C-methyl-D-erythritol 4-phosphate pathway. Planta Med 72:329–335

    Article  CAS  PubMed  Google Scholar 

  • Goral TK, Johnson MP, Duffy CD, Brain AP, Ruban AV, Mullineaux CW (2012) Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. Plant J 69:289–301

    Article  CAS  PubMed  Google Scholar 

  • He Q, Jones DC, Li W, Xie F, Ma J, Sun R, Wang Q, Zhu S, Zhang B (2016) Genome-wide identification of R2R3-MYB genes and expression analyses during abiotic stress in Gossypium raimondii. Sci Rep 6:22980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V (2011) Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J Exp Bot 62:erq442

    Article  Google Scholar 

  • Higginson T, Li SF, Parish RW (2003) AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. Plant J 35:177–192

    Article  CAS  PubMed  Google Scholar 

  • Hricova A, Fejer J, Libiakova G, Szabova M, Gazo J, Gajdosova A (2016) Characterization of phenotypic and nutritional properties of valuable Amaranthus cruentus L. mutants. Turk J Agric For 40:761–771

    Article  Google Scholar 

  • Jakoby MJ, Falkenhan D, Mader MT, Brininstool G, Wischnitzki E, Platz N, Hudson A, Hülskamp M, Larkin J, Schnittger A (2008) Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-like transcriptional regulator MYB106. Plant Physiol 148:1583–1602

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Jung C, Seo JS, Han SW, Koo YJ, Kim CH, Song SI, Nahm BH, Do Choi Y, Cheong JJ (2008) Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146:623–635

    Article  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 13:544–582

    Article  CAS  Google Scholar 

  • Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lee D-K, Geisler M, Springer PS (2009) LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis. Development 136:2423–2432

    Article  CAS  PubMed  Google Scholar 

  • Li C, Lu S (2014) Genome-wide characterization and comparative analysis of R2R3-MYB transcription factors shows the complexity of MYB-associated regulatory networks in Salvia miltiorrhiza. BMC Genom 15:277

    Article  Google Scholar 

  • Li L, Cheng H, Yuan H, Xu F, Cheng S, Cao F (2014) Functional characterization of the Ginkgo biloba chalcone synthase gene promoter in transgenic tobacco. Genet Mol Res 13:3446–3460

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM (2005) AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol 15:1201–1206

    Article  CAS  PubMed  Google Scholar 

  • Liao YL, Shen YB, Jie C, Zhang WW, Cheng SY, Feng X (2015) Isolation, expression, and promoter analysis of GbWRKY2: a novel transcription factor gene from Ginkgo biloba. Int J Genomics 2015:607185

    Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Liu R, Lü B, Wang X, Zhang C, Zhang S, Qian J, Chen L, Shi H, Dong H (2010) Thirty-seven transcription factor genes differentially respond to a harpin protein and affect resistance to the green peach aphid in Arabidopsis. J Biosci 35:435–450

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Matus JT, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8:83

    Article  PubMed  PubMed Central  Google Scholar 

  • Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113

    Article  CAS  PubMed  Google Scholar 

  • Nakatsuka A, Yamagishi M, Nakano M, Tasaki K, Kobayashi N (2009) Light-induced expression of basic helix-loop-helix genes involved in anthocyanin biosynthesis in flowers and leaves of Asiatic hybrid lily. Sci Hortic 121:84–91

    Article  CAS  Google Scholar 

  • Newman LJ, Perazza DE, Juda L, Campbell MM (2004) Involvement of the R2R3-MYB, AtMYB61, in the ectopic lignification and dark-photomorphogenic components of the det3 mutant phenotype. Plant J 37:239–250

    Article  CAS  PubMed  Google Scholar 

  • Novo-Uzal E, Gutiérrez J, Martínez-Cortés T, Pomar F (2014) Molecular cloning of two novel peroxidases and their response to salt stress and salicylic acid in the living fossil Ginkgo biloba. Ann Bot 114:923–936

    Article  PubMed  PubMed Central  Google Scholar 

  • Ogata K, Hojo H, Aimoto S, Nakai T, Nakamura H, Sarai A, Ishii S, Nishimura Y (1992) Solution structure of a DNA-binding unit of Myb: a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc Natl Acad Sci 89:6428–6432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogata K, Morikawa S, Nakamura H, Sekikawa A, Inoue T, Kanai H, Sarai A, Ishii S, Nishimura Y (1994) Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell 79:639–648

    Article  CAS  PubMed  Google Scholar 

  • Ogata K, Morikawa S, Nakamura H, Hojo H, Yoshimura S, Zhang R, Aimoto S, Ametani Y, Hirata Z, Sarai A (1995) Comparison of the free and DNA-complexed forms of the DMA-binding domain from c-Myb. Nat Struct Mol Biol 2:309–320

    Article  CAS  Google Scholar 

  • Ogatallz K, Kanei-Ishiil C, Sasakiz M, Hatanaka H, Nagadoiz A, Enariz M, Nakamura H, Nishimuraz Y (1996) The cavity in the hydrophobic core of Myb DNA-binding domain is reserved for DNA. Nat Struct Biol 3:178–187

    Article  Google Scholar 

  • Pasternak D (1987) Salt tolerance and crop production-a comprehensive approach. Annu Rev Phytopathol 25:271–291

    Article  Google Scholar 

  • Paz-Ares J, Ghosal D, Wienand U, Peterson P, Saedler H (1987) 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 

  • Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C (2005) Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132:359–370

    Article  CAS  PubMed  Google Scholar 

  • Rabinowicz PD, Braun EL, Wolfe AD, Bowen B, Grotewold E (1999) Maize R2R3 Myb genes: sequence analysis reveals amplification in the higher plants. Genetics 153:427–444

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Royer DL, Hickey LJ, Wing SL (2003) Ecological conservatism in the “living fossil” Ginkgo. J Inf 29:84–104

    Google Scholar 

  • Sakar E, Unver H, Bakir M, Ulas M, Sakar ZM (2016) Genetic relationships among olive (Olea europaea L.) cultivars native to Turkey. Biochem Genet 54:348–359

    Article  CAS  PubMed  Google Scholar 

  • Saridas MA, Kafkas NE, Zarifikhosroshahi M, Bozhaydar O, Kargi SP (2016) Quality traits of green plums (Prunus cerasifera Ehrh.) at different maturity stages. Turk J Agric For 40:655–663

    Article  Google Scholar 

  • Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483

    Article  CAS  PubMed  Google Scholar 

  • Shen G, Pang Y, Wu W, Liao Z, Zhao L, Sun X, Tang K (2006) Cloning and characterization of a root-specific expressing gene encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase from Ginkgo biloba. Mol Biol Rep 33:117–127

    Article  CAS  PubMed  Google Scholar 

  • Shin B, Choi G, Yi H, Yang S, Cho I, Kim J, Lee S, Paek NC, Kim JH, Song PS (2002) AtMYB21, a gene encoding a flower-specific transcription factor, is regulated by COP1. Plant J 30:23–32

    Article  CAS  PubMed  Google Scholar 

  • Singh UM, Chandra M, Shankhdhar SC, Kumar A (2014) Transcriptome wide identification and validation of calcium sensor gene family in the developing spikes of finger millet genotypes for elucidating its role in grain calcium accumulation. PLoS ONE 9:e103963

    Article  PubMed  PubMed Central  Google Scholar 

  • Solmaz I, Kacar Y, Simsek O, Sari N (2016) Genetic characterization of turkish snake melon (Cucumis melo L. subsp. melo flexuosus Group) accessions revealed by SSR markers. Biochem Genet 54:534–543

    Article  CAS  PubMed  Google Scholar 

  • Steiner-Lange S, Unte US, Eckstein L, Yang C, Wilson ZA, Schmelzer E, Dekker K, Saedler H (2003) Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J 34:519–528

    Article  CAS  PubMed  Google Scholar 

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

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stracke R, Holtgräwe D, Schneider J, Pucker B, Sörensen TR, Weisshaar B (2014) Genome-wide identification and characterisation of R2R3-MYB genes in sugar beet (Beta vulgaris). BMC Plant Biol 14:249

    Article  PubMed  PubMed Central  Google Scholar 

  • Tombuloglu H, Kekec G, Sakcali MS, Unver T (2013) Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis. Mol Genet Genomics 288:141–155

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Tang J, Hu R, Wu P, Hou X, Song X, Xiong A (2015) Genome-wide analysis of the R2R3-MYB transcription factor genes in Chinese cabbage (Brassica rapa ssp. pekinensis) reveals their stress and hormone responsive patterns. BMC Genom 16:17

    Article  Google Scholar 

  • Wasternack C, Hause B (2002) Jasmonates and octadecanoids: signals in plant stress responses and development. Prog Nucleic Acid Res Mol Biol 72:165–221

    Article  CAS  PubMed  Google Scholar 

  • Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu C, Huang H, Yeh L-SL, Barker WC (2003a) Protein family classification and functional annotation. Comput Biol Chem 27:37–47

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Lim SH, Yang W (2003b) Characterization, expression and phylogenetic study of R2R3-MYB genes in orchid. Plant Mol Biol 51:959–972

    Article  CAS  PubMed  Google Scholar 

  • Xie R, Zheng L, Deng L, He S, Yi S, Lv Q, Zheng Y (2014) The role of R2R3MYB transcription factors in plant stress tolerance. J Anim Plant Sci 24:1821–1833

    Google Scholar 

  • Xu F, Cheng H, Cai R, Li LL, Chang J, Zhu J, Zhang FX, Chen LJ, Wang Y, Cheng SH (2008) Molecular cloning and function analysis of an anthocyanidin synthase gene from Ginkgo biloba, and its expression in abiotic stress responses. Mol Cells 26:536–547

    CAS  PubMed  Google Scholar 

  • Xu F, Li L, Zhang W, Cheng H, Sun N, Cheng S, Wang Y (2012) Isolation, characterization, and function analysis of a flavonol synthase gene from Ginkgo biloba. Mol Biol Rep 39:2285–2296

    Article  CAS  PubMed  Google Scholar 

  • Xu F, Ning Y, Zhang W, Liao Y, Li L, Cheng H, Cheng S (2014) An R2R3-MYB transcription factor as a negative regulator of the flavonoid biosynthesis pathway in Ginkgo biloba. Funct Integr Genomics 14:177–189

    Article  PubMed  Google Scholar 

  • Zhang Y, Cao G, Qu L, Gu H (2009) Characterization of Arabidopsis MYB transcription factor gene AtMYB17 and its possible regulation by LEAFY and AGL15. J Genet Genomics 36:99–107

    Article  PubMed  Google Scholar 

  • Zhang L, Chen J, Li Q, Chen W (2016) Transcriptome-wide analysis of basic helix-loop-helix transcription factors in Isatis indigotica and their methyl jasmonate responsive expression profiling. Gene 576:150–159

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Gao L, Wang H, Chen X, Wang Y, Yang H, Wei C, Wan X, Xia T (2013) The R2R3-MYB, bHLH, WD40, and related transcription factors in flavonoid biosynthesis. Funct Integr Genomics 13:75–98

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Lee C, Zhong R, Ye Z (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266

    Article  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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Forestry Industry Research Special Funds for Public Welfare Projects (201504105), Jiangsu Postdoctoral Science Foundation (1401062B), Colleges and Universities in Jiangsu Province Plans to Graduate Research and Innovation (CXZZ13_0552), and Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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  1. Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, 210037, China

    Xinliang Liu, Wanwen Yu, Xuhui Zhang, Guibin Wang & Fuliang Cao

  2. Jiangxi Academy of Forestry, Nanchang, 330032, China

    Xinliang Liu

  3. The Jiangsu Provincial Platform for Conservation and Utilization of Agricultural Germplasm, Nanjing, 210037, China

    Wanwen Yu

  4. Economic Forest Germplasm Improvement and Comprehensive Utilization of Resources of Hubei Key Laboratories, Huanggang Normal University, Huanggang, 438000, China

    Hua Cheng

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  1. Xinliang Liu
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Correspondence to Fuliang Cao.

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Liu, X., Yu, W., Zhang, X. et al. Identification and expression analysis under abiotic stress of the R2R3-MYB genes in Ginkgo biloba L.. Physiol Mol Biol Plants 23, 503–516 (2017). https://doi.org/10.1007/s12298-017-0436-9

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