Skip to main content
SpringerLink
Log in

Regulatory Sequences in Apple

  • Chapter
  • First Online:
The Apple Genome

Part of the book series: Compendium of Plant Genomes ((CPG))

  • 1153 Accesses

Abstract

Apple (Malus × domestica Borkh.) is one of the most important cultivated fruit trees in the world. However, studies on apple gene regulation have long lagged behind model plants due to incomplete information on the genome sequence. This has limited identification and functional characterization of regulatory sequences, that is, numbers, types, and functional roles of genes involved in the regulation of various biological processes in the apple. In general, regulatory sequences can either promote or repress the expression of downstream genes through different regulatory mechanisms, such as protein–DNA binding or protein–protein interactions. Gene expression is highly regulated at the transcriptional level. As a primary type of regulatory sequences, transcription factors (TFs) play critical roles in this process by either positively or negatively regulating the expression of multiple genes, including both downstream structural genes and other regulatory sequences. TFs regulate gene expression by interacting with specific cis-elements in target genes and by forming protein complexes with other TFs to either promote or suppress target gene expression in regulatory modules. Over the past decade, apple whole-genome sequencing efforts have enabled the collection of genomic information on apple TF families and their specific roles in regulation of fruit quality traits, abiotic and biotic stress resistance, and various other important biological traits. In this chapter, we will provide an introduction of apple TFs, and review recent studies on their roles in the regulation of apple growth and development.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allan AC, Espley RV (2018) MYBs drive novel consumer traits in fruits and vegetables. Trends Plant Sci 23(8):693–705

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF (2000) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 24(4):457–466

    Article  CAS  PubMed  Google Scholar 

  • An X-H, Tian Y, Chen K-Q, Liu X-J, Liu D-D, Xie X-B, Cheng C-G, Cong P-H, Hao Y-J (2015) MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant Cell Physiol 56(4):650–662

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Li H-H, Song L-Q, Su L, Liu X, You C-X, Wang X-F, Hao Y-J (2016) The molecular cloning and functional characterization of MdMYC2, a bHLH transcription factor in apple. Plant Physiol Biochem 108:24–31

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Liu X, Li H-H, You C-X, Wang X-F, Hao Y-J (2017a) Apple RING E3 ligase MdMIEL1 inhibits anthocyanin accumulation by ubiquitinating and degrading MdMYB1 protein. Plant Cell Physiol 58(11):1953–1962

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Qu F-J, Yao J-F, Wang X-N, You C-X, Wang X-F, Hao Y-J (2017b) The bZIP transcription factor MdHY5 regulates anthocyanin accumulation and nitrate assimilation in apple. Hortic Res 4(1):1–9

    Google Scholar 

  • An J-P, Wang X-N, Yao J-F, Ren Y-R, You C-X, Wang X-F, Hao Y-J (2017c) Apple MdMYC2 reduces aluminum stress tolerance by directly regulating MdERF3 gene. Plant Soil 418(1–2):255–266

    Article  CAS  Google Scholar 

  • An J-P, Yao J-F, Wang X-N, You C-X, Wang X-F, Hao Y-J (2017d) MdHY5 positively regulates cold tolerance via CBF-dependent and CBF-independent pathways in apple. J Plant Physiol 218:275–281

    Article  CAS  PubMed  Google Scholar 

  • An J-P, An X-H, Yao J-F, Wang X-N, You C-X, Wang X-F, Hao Y-J (2018a) BTB protein MdBT2 inhibits anthocyanin and proanthocyanidin biosynthesis by triggering MdMYB9 degradation in apple. Tree Physiol 38(10):1578–1587

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Li R, Qu F-J, You C-X, Wang X-F, Hao Y-J (2018b) An apple NAC transcription factor negatively regulates cold tolerance via CBF-dependent pathway. J Plant Physiol 221:74–80

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Li R, Qu F-J, You C-X, Wang X-F, Hao Y-J (2018c) R2R3-MYB transcription factor MdMYB23 is involved in the cold tolerance and proanthocyanidin accumulation in apple. Plant J 96(3):562–577

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Wang X-F, Li Y-Y, Song L-Q, Zhao L-L, You C-X, Hao Y-J (2018d) EIN3-LIKE1, MYB1, and ETHYLENE RESPONSE FACTOR3 act in a regulatory loop that synergistically modulates ethylene biosynthesis and anthocyanin accumulation. Plant Physiol 178(2):808–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An J-P, Yao J-F, Xu R-R, You C-X, Wang X-F, Hao Y-J (2018e) An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response. Physiol Plant 164(3):279–289

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Yao J-F, Xu R-R, You C-X, Wang X-F, Hao Y-J (2018f) Apple bZIP transcription factor MdbZIP44 regulates abscisic acid-promoted anthocyanin accumulation. Plant Cell Environ 41(11):2678–2692

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Zhang X-W, Xu R-R, You C-X, Wang X-F, Hao Y-J (2018g) Apple MdERF4 negatively regulates salt tolerance by inhibiting MdERF3 transcription. Plant Sci 276:181–188

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Wang X-F, Zhang X-W, Bi S-Q, You C-X, Hao Y-J (2019a) MdBBX22 regulates UV-B-induced anthocyanin biosynthesis through regulating the function of MdHY5 and is targeted by MdBT2 for 26S proteasome-mediated degradation. Plant Biotechnol J 17(12):2231–2233

    Article  PubMed  PubMed Central  Google Scholar 

  • An J-P, Zhang X-W, Bi S-Q, You C-X, Wang X-F, Hao Y-J (2019b) MdbHLH93, an apple activator regulating leaf senescence, is regulated by ABA and MdBT2 in antagonistic ways. New Phytol 222(2):735–751

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Zhang X-W, You C-X, Bi S-Q, Wang X-F, Hao Y-J (2019c) MdWRKY40 promotes wounding-induced anthocyanin biosynthesis in association with MdMYB1 and undergoes MdBT2-mediated degradation. New Phytol 224(1):380–395

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Liu Y-H, Zhang X-W, Bi S-Q, Wang X-F, You C-X, Hao Y-J (2020a) Dynamic regulation of different light intensity-modulated anthocyanin biosynthesis by BT2-TCP46-MYB1 in apple. J Exp Bot 71(10):3094–3109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An J-P, Wang X-F, Espley RV, Lin-Wang K, Bi S-Q, You C-X, Hao Y-J (2020b) An apple B-Box protein MdBBX37 modulates anthocyanin biosynthesis and hypocotyl elongation synergistically with MdMYBs and MdHY5. Plant Cell Physiol 61(1):130–143

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Wang X-F, Hao Y-J (2020c) BTB/TAZ protein MdBT2 integrates multiple hormonal and environmental signals to regulate anthocyanin biosynthesis in apple. J Integr Plant Biol 62(11):1643–1646

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Wang X-F, Zhang X-W, Xu H-F, Bi S-Q, You C-X, Hao Y-J (2020d) An apple MYB transcription factor regulates cold tolerance and anthocyanin accumulation and undergoes MIEL1-mediated degradation. Plant Biotechnol J 18(2):337–353

    Article  CAS  PubMed  Google Scholar 

  • An J-P, Zhang X-W, Bi S-Q, You C-X, Wang X-F, Hao Y-J (2020e) The ERF transcription factor MdERF38 promotes drought stress-induced anthocyanin biosynthesis in apple. Plant J 101(3):573–589

    Article  CAS  PubMed  Google Scholar 

  • Bai S, Saito T, Honda C, Hatsuyama Y, Ito A, Moriguchi T (2014) An apple B-box protein, MdCOL11, is involved in UV-B-and temperature-induced anthocyanin biosynthesis. Planta 240(5):1051–1062

    Article  CAS  PubMed  Google Scholar 

  • Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29(3):464–489

    Article  CAS  PubMed  Google Scholar 

  • Boeva V (2016) Analysis of genomic sequence motifs for deciphering transcription factor binding and transcriptional regulation in eukaryotic cells. Front Genet 7:24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bolger ME, Weisshaar B, Scholz U, Stein N, Usadel B, Mayer KF (2014) Plant genome sequencing-applications for crop improvement. Curr Opin Biotechnol 26:31–37

    Article  CAS  PubMed  Google Scholar 

  • Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12(12):2383–2393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brand LH, Fischer NM, Harter K, Kohlbacher O, Wanke D (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res 41(21):9764–9778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao Z-H, Zhang S-Z, Wang R-K, Zhang R-F, Hao Y-J (2013) Genome wide analysis of the apple MYB transcription factor family allows the identification of MdoMYB121 gene conferring abiotic stress tolerance in plants. PLoS ONE 8(7):e69955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cevik V, Ryder CD, Popovich A, Manning K, King GJ, Seymour GB (2010) A FRUITFULL-like gene is associated with genetic variation for fruit flesh firmness in apple (Malus domestica Borkh.). Tree Genet Genomes 6(2):271–279

    Google Scholar 

  • Chagné D, Lin-Wang K, Espley RV, Volz RK, How NM, Rouse S, Brendolise C, Carlisle CM, Kumar S, De Silva N (2013) An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiol 161(1):225–239

    Article  PubMed  CAS  Google Scholar 

  • Chen F, Hu Y, Vannozzi A, Wu K, Cai H, Qin Y, Mullis A, Lin Z, Zhang L (2017a) The WRKY transcription factor family in model plants and crops. Crit Rev Plant Sci 36(5–6):311–335

    Article  Google Scholar 

  • Chen H, Shao H, Li K, Zhang D, Fan S, Li Y, Han M (2017b) Genome-wide identification, evolution, and expression analysis of GATA transcription factors in apple (Malus × domestica Borkh.). Gene 627:460–472

    Article  CAS  PubMed  Google Scholar 

  • Chen K, Song M, Guo Y, Liu L, Xue H, Dai H, Zhang Z (2019) MdMYB46 could enhance salt and osmotic stress tolerance in apple by directly activating stress-responsive signals. Plant Biotechnol J 17(12):2341–2355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daccord N, Celton J-M, Linsmith G, Becker C, Choisne N, Schijlen E, Van de Geest H, Bianco L, Micheletti D, Velasco R (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49(7):1099–1106

    Article  CAS  PubMed  Google Scholar 

  • Dash M, Malladi A (2012) The AINTEGUMENTA genes, MdANT1 and MdANT2, are associated with the regulation of cell production during fruit growth in apple (Malus × domestica Borkh.). BMC Plant Biol 12(1):98. https://doi.org/10.1186/1471-2229-12-98

  • Davuluri RV, Sun H, Palaniswamy SK, Matthews N, Molina C, Kurtz M, Grotewold E (2003) AGRIS: Arabidopsis gene regulatory information server, an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinformatics 4(1):25. https://doi.org/10.1186/1471-2105-4-25

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong Y-H, Yao J-L, Atkinson RG, Putterill JJ, Morris BA, Gardner RC (2000) MDH1: an apple homeobox gene belonging to the BEL1 family. Plant Mol Biol 42(4):623–633

    Article  CAS  PubMed  Google Scholar 

  • Duan N, Bai Y, Sun H, Wang N, Ma Y, Li M, Wang X, Jiao C, Legall N, Mao L (2017) Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat Commun 8(1):249. https://doi.org/10.1038/s41467-017-00336-7

    Article  CAS  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(10):573–581

    Article  CAS  PubMed  Google Scholar 

  • Espley RV, Brendolise C, Chagné D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten HJ, Gardiner SE, Hellens RP (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell 21(1):168–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199–206

    Article  CAS  PubMed  Google Scholar 

  • Fang H, Dong Y, Yue X, Chen X, He N, Hu J, Jiang S, Xu H, Wang Y, Su M (2019a) MdCOL4 interaction mediates crosstalk between UV-B and high temperature to control fruit coloration in apple. Plant Cell Physiol 60(5):1055–1066

    Article  CAS  PubMed  Google Scholar 

  • Fang H, Dong Y, Yue X, Hu J, Jiang S, Xu H, Wang Y, Su M, Zhang J, Zhang Z (2019b) The B-box zinc finger protein MdBBX20 integrates anthocyanin accumulation in response to ultraviolet radiation and low temperature. Plant Cell Environ 42(7):2090–2104

    Article  CAS  PubMed  Google Scholar 

  • Fan H, Wang F, Gao H, Wang L, Xu J, Zhao Z (2011) Pathogen-induced MdWRKY1 in ‘Qinguan’ apple enhances disease resistance. J Plant Biol 54(3):150–158

    Article  CAS  Google Scholar 

  • Feng X-M, Zhao Q, Zhao L-L, Qiao Y, Xie X-B, Li H-F, Yao Y-X, You C-X, Hao Y-J (2012) The cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1 encodes an ICE-like protein in apple. BMC Plant Biol 12(1):22. https://doi.org/10.1186/1471-2229-12-22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flachowsky H, Hättasch C, Höfer M, Peil A, Hanke M-V (2010) Overexpression of LEAFY in apple leads to a columnar phenotype with shorter internodes. Planta 231(2):251–263

    Article  CAS  PubMed  Google Scholar 

  • Gangappa SN, Botto JF (2014) The BBX family of plant transcription factors. Trends Plant Sci 19(7):460–470

    Article  CAS  PubMed  Google Scholar 

  • Gao J-J, Zhang Z, Peng R-H, Xiong A-S, Xu J, Zhu B, Yao Q-H (2011) Forced expression of Mdmyb10, a myb transcription factor gene from apple, enhances tolerance to osmotic stress in transgenic Arabidopsis. Mol Biol Rep 38(1):205–211

    Article  CAS  PubMed  Google Scholar 

  • Girardi CL, Rombaldi CV, Dal Cero J, Nobile PM, Laurens F, Bouzayen M, Quecini V (2013) Genome-wide analysis of the AP2/ERF superfamily in apple and transcriptional evidence of ERF involvement in scab pathogenesis. Sci Hortic 151:112–121

    Article  CAS  Google Scholar 

  • Guilfoyle TJ, Ulmasov T, Hagen G (1998) The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol Life Sci 54(7):619–627

    Article  CAS  PubMed  Google Scholar 

  • Gu K-D, Wang C-K, Hu D-G, Hao Y-J (2019) How do anthocyanins paint our horticultural products? Sci Hortic 249:257–262

    Article  CAS  Google Scholar 

  • Han Z, Hu Y, Lv Y, Rose JK, Sun Y, Shen F, Wang Y, Zhang X, Xu X, Wu T (2018) Natural variation underlies differences in ETHYLENE RESPONSE FACTOR17 activity in fruit peel degreening. Plant Physiol 176(3):2292–2304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henschel K, Kofuji R, Hasebe M, Saedler H, Münster T, Theissen G (2002) Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol Biol Evol 19(6):801–814

    Article  CAS  PubMed  Google Scholar 

  • Honda C, Moriya S (2018) Anthocyanin biosynthesis in apple fruit. Hortic J 87(3):305–314

    Article  CAS  Google Scholar 

  • Hu JC, Sauer R (1992) The basic-region leucine-zipper family of DNA binding proteins. Nucleic acids and molecular biology. Springer, New York, NY, pp 82–101

    Chapter  Google Scholar 

  • Hu D-G, Sun C-H, Ma Q-J, You C-X, Cheng L, Hao Y-J (2016a) MdMYB1 regulates anthocyanin and malate accumulation by directly facilitating their transport into vacuoles in apples. Plant Physiol 170(3):1315–1330

    Article  CAS  PubMed  Google Scholar 

  • Hu D-G, Sun C-H, Zhang Q-Y, An J-P, You C-X, Hao Y-J (2016b) Glucose sensor MdHXK1 phosphorylates and stabilizes MdbHLH3 to promote anthocyanin biosynthesis in apple. PLoS Genet 12(8):e1006273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hu D-G, Li Y-Y, Zhang Q-Y, Li M, Sun C-H, Yu J-Q, Hao Y-J (2017) The R2R3-MYB transcription factor MdMYB73 is involved in malate accumulation and vacuolar acidification in apple. Plant J 91(3):443–454

    Article  CAS  PubMed  Google Scholar 

  • Hu D-G, Yu J-Q, Han P-L, Xie X-B, Sun C-H, Zhang Q-Y, Wang J-H, Hao Y-J (2019) The regulatory module MdPUB29-MdbHLH3 connects ethylene biosynthesis with fruit quality in apple. New Phytol 221(4):1966–1982

    Article  CAS  PubMed  Google Scholar 

  • Ireland HS, Yao J-L, Tomes S, Sutherland PW, Nieuwenhuizen N, Gunaseelan K, Winz RA, David KM, Schaffer RJ (2013) Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant J 73(6):1044–1056

    Article  CAS  PubMed  Google Scholar 

  • Jia D, Gong X, Li M, Li C, Sun T, Ma F (2018a) Overexpression of a novel apple NAC transcription factor gene, MdNAC1, confers the dwarf phenotype in transgenic apple (Malus domestica). Genes 9(5):229

    Article  PubMed Central  CAS  Google Scholar 

  • Jia D, Shen F, Wang Y, Wu T, Xu X, Zhang X, Han Z (2018b) Apple fruit acidity is genetically diversified by natural variations in three hierarchical epistatic genes: MdSAUR37, MdPP2CH and MdALMTII. Plant J 95(3):427–443

    Article  CAS  PubMed  Google Scholar 

  • Jia D, Jiang Q, van Nocker S, Gong X, Ma F (2019) An apple (Malus domestica) NAC transcription factor enhances drought tolerance in transgenic apple plants. Plant Physiol Biochem 139:504–512

    Article  CAS  PubMed  Google Scholar 

  • Jin J, Tian F, Yang D-C, Meng Y-Q, 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(D1):D1040-D1045. https://doi.org/10.1093/nar/gkw982

  • Kavas M, Baloğlu MC, Atabay ES, Ziplar UT, Daşgan HY, Ünver T (2016) Genome-wide characterization and expression analysis of common bean bHLH transcription factors in response to excess salt concentration. Mol Genet Genomics 291(1):129–143

    Article  CAS  PubMed  Google Scholar 

  • Kotoda N, Wada M, Kusaba S, Kano-Murakami Y, Masuda T, Soejima J (2002) Overexpression of MdMADS5, an APETALA1-like gene of apple, causes early flowering in transgenic Arabidopsis. Plant Sci 162(5):679–687

    Article  CAS  Google Scholar 

  • Kumar G, Arya P, Gupta K, Randhawa V, Acharya V, Singh AK (2016) Comparative phylogenetic analysis and transcriptional profiling of MADS-box gene family identified DAM and FLC-like genes in apple (Malus × domestica). Sci Rep 6(1):1–13

    CAS  Google Scholar 

  • Lashbrooke J, Aharoni A, Costa F (2015) Genome investigation suggests MdSHN3, an APETALA2-domain transcription factor gene, to be a positive regulator of apple fruit cuticle formation and an inhibitor of russet development. J Exp Bot 66(21):6579–6589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legay S, Guerriero G, André C, Guignard C, Cocco E, Charton S, Boutry M, Rowland O, Hausman JF (2016) MdMyb93 is a regulator of suberin deposition in russeted apple fruit skins. New Phytol 212(4):977–991

    Article  CAS  PubMed  Google Scholar 

  • Liao X, Guo X, Wang Q, Wang Y, Zhao D, Yao L, Wang S, Liu G, Li T (2017) Overexpression of MsDREB6.2 results in cytokinin-deficient developmental phenotypes and enhances drought tolerance in transgenic apple plants. Plant J 89(3):510–526

    Google Scholar 

  • Liu X, Li R, Dai Y, Chen X, Wang X (2018) Genome-wide identification and expression analysis of the B-box gene family in the apple (Malus domestica Borkh.) genome. Mol Genet Genomics 293(2):303–315

    Google Scholar 

  • Liu W, Wang Y, Sun J, Jiang H, Xu H, Wang N, Jiang S, Fang H, Zhang Z, Wang Y-L (2019a) MdMYBDL1 employed by MdHY5 increases anthocyanin accumulation via repression of MdMYB16/308 in apple. Plant Sci 283:32–40. https://doi.org/10.1016/j.plantsci.2019.01.016

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Wang Y, Yu L, Jiang H, Guo Z, Xu H, Jiang S, Fang H, Zhang J, Su M (2019b) MdWRKY11 participates in anthocyanin accumulation in red-fleshed apples by affecting MYB transcription factors and the photoresponse factor MdHY5. J Agric Food Chem 67(32):8783–8793

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Li R, Dai Y, Yuan L, Sun Q, Zhang S, Wang X (2019c) A B-box zinc finger protein, MdBBX10, enhanced salt and drought stresses tolerance in Arabidopsis. Plant Mol Biol 99(4–5):437–447

    Article  CAS  PubMed  Google Scholar 

  • Li Y-Y, Mao K, Zhao C, Zhao X-Y, Zhang H-L, Shu H-R, Hao Y-J (2012) MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple. Plant Physiol 160(2):1011–1022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Hou H, Li X, Xiang J, Yin X, Gao H, Zheng Y, Bassett CL, Wang X (2013) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus × domestica Borkh.). Plant Physiol Biochem 70:100–114

    Article  CAS  PubMed  Google Scholar 

  • Li T, Jiang Z, Zhang L, Tan D, Wei Y, Yuan H, Li T, Wang A (2016a) Apple (Malus domestica) MdERF2 negatively affects ethylene biosynthesis during fruit ripening by suppressing MdACS1 transcription. Plant J 88(5):735–748

    Article  CAS  PubMed  Google Scholar 

  • Li Y-Y, Meng D, Li M, Cheng L (2016b) Genome-wide identification and expression analysis of the bZIP gene family in apple (Malus domestica). Tree Genet Genomes 12(4):82. https://doi.org/10.1007/s11295-016-1043-6

    Article  Google Scholar 

  • Li H-H, Liu X, An J-P, Hao Y-J, Wang X-F, You C-X (2017a) Cloning and elucidation of the functional role of apple MdLBD13 in anthocyanin biosynthesis and nitrate assimilation. Plant Cell Tiss Org Cult (PCTOC) 130(1):47–59

    Article  CAS  Google Scholar 

  • Li T, Xu Y, Zhang L, Ji Y, Tan D, Yuan H, Wang A (2017b) The jasmonate-activated transcription factor MdMYC2 regulates ETHYLENE RESPONSE FACTOR and ethylene biosynthetic genes to promote ethylene biosynthesis during apple fruit ripening. Plant Cell 29(6):1316–1334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Xie Y, Lu L, Yan M, Fang N, Xu J, Wang L, Yan Y, Zhao T, van Nocker S (2019) Contribution of methylation regulation of MpDREB2A promoter to drought resistance of Mauls prunifolia. Plant Soil 441:15–32. https://doi.org/10.1007/s11104-019-04149-z

    Article  CAS  Google Scholar 

  • Li C, Meng D, Pineros MA, Mao Y, Dandekar AM, Cheng L (2020) A sugar transporter takes up both hexose and sucrose for sorbitol-modulated in vitro pollen tube growth in apple. Plant Cell 32(2):449–469

    Article  CAS  PubMed  Google Scholar 

  • Lui S, Luo C, Zhu L, Sha R, Qu S, Cai B, Wang S (2017) Identification and expression analysis of WRKY transcription factor genes in response to fungal pathogen and hormone treatments in apple (Malus domestica). J Plant Biol 60(2):215–230

    Article  CAS  Google Scholar 

  • Luo X-C, Sun M-H, Xu R-R, Shu H-R, Wang J-W, Zhang S-Z (2014) Genomewide identification and expression analysis of the ARF gene family in apple. J Genet 93(3):785–797

    Article  PubMed  Google Scholar 

  • Mao K, Dong Q, Li C, Liu C, Ma F (2017) Genome wide identification and characterization of apple bHLH transcription factors and expression analysis in response to drought and salt stress. Front Plant Sci 8:480. https://doi.org/10.3389/fpls.2017.00480

    Article  PubMed  PubMed Central  Google Scholar 

  • Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20(2):429–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Q-J, Sun M-H, Lu J, Liu Y-J, Hu D-G, Hao Y-J (2017) Transcription factor AREB2 is involved in soluble sugar accumulation by activating sugar transporter and amylase genes. Plant Physiol 174(4):2348–2362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng D, Li Y, Bai Y, Li M, Cheng L (2016) Genome-wide identification and characterization of WRKY transcriptional factor family in apple and analysis of their responses to waterlogging and drought stress. Plant Physiol Biochem 103:71–83

    Article  CAS  PubMed  Google Scholar 

  • Meng D, He M, Bai Y, Xu H, Dandekar AM, Fei Z, Cheng L (2018a) Decreased sorbitol synthesis leads to abnormal stamen development and reduced pollen tube growth via an MYB transcription factor, MdMYB39L, in apple (Malus domestica). New Phytol 217(2):641–656

    Article  CAS  PubMed  Google Scholar 

  • Meng D, Li C, Park H-J, González J, Wang J, Dandekar AM, Turgeon BG, Cheng L (2018b) Sorbitol modulates resistance to Alternaria alternata by regulating the expression of an NLR resistance gene in apple. Plant Cell 30(7):1562–1581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10(2):79–87

    Article  CAS  PubMed  Google Scholar 

  • Orenstein Y, Shamir R (2016) Modeling protein-DNA binding via high-throughput in vitro technologies. Brief Funct Genomics 16(3):171–180

    PubMed Central  Google Scholar 

  • Osakabe Y, Liang Z, Ren C, Nishitani C, Osakabe K, Wada M, Komori S, Malnoy M, Velasco R, Poli M (2018) CRISPR-Cas9-mediated genome editing in apple and grapevine. Nat Protoc 13(12):2844–2863

    Article  CAS  PubMed  Google Scholar 

  • Peace CP, Bianco L, Troggio M, Van de Weg E, Howard NP, Cornille A, Durel C-E, Myles S, Migicovsky Z, Schaffer RJ (2019) Apple whole genome sequences: recent advances and new prospects. Hortic Res 6(1):1–24

    Article  Google Scholar 

  • Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:760. https://doi.org/10.3389/fpls.2016.00760

    Article  PubMed  PubMed Central  Google Scholar 

  • Riechmann JL, Ratcliffe OJ (2000) A genomic perspective on plant transcription factors. Curr Opin Plant Biol 3(5):423–434

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem Biophys Res Commun 290(3):998–1009

    Article  CAS  PubMed  Google Scholar 

  • Samad AF, Sajad M, Nazaruddin N, Fauzi IA, Murad A, Zainal Z, Ismail I (2017) MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci 8:565. https://doi.org/10.3389/fpls.2017.00565

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma V, Goel P, Kumar S, Singh AK (2019) An apple transcription factor, MdDREB76, confers salt and drought tolerance in transgenic tobacco by activating the expression of stress-responsive genes. Plant Cell Rep 38(2):221–241

    Article  CAS  PubMed  Google Scholar 

  • Sung S-K, Yu G-H, An G (1999) Characterization of MdMADS2, a member of the SQUAMOSA subfamily of genes, in apple. Plant Physiol 120(4):969–978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Q, Jiang S, Zhang T, Xu H, Fang H, Zhang J, Su M, Wang Y, Zhang Z, Wang N (2019) Apple NAC transcription factor MdNAC52 regulates biosynthesis of anthocyanin and proanthocyanidin through MdMYB9 and MdMYB11. Plant Sci 289:110286. https://doi.org/10.1016/j.plantsci.2019.110286

    Article  CAS  PubMed  Google Scholar 

  • Su H, Zhang S, Yuan X, Chen C, Wang X-F, Hao Y-J (2013) Genome-wide analysis and identification of stress-responsive genes of the NAM-ATAF1,2-CUC2 transcription factor family in apple. Plant Physiol Biochem 71:11–21

    Article  CAS  PubMed  Google Scholar 

  • Tian Y, Dong Q, Ji Z, Chi F, Cong P, Zhou Z (2015) Genome-wide identification and analysis of the MADS-box gene family in apple. Gene 555(2):277–290

    Article  CAS  PubMed  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15(2):533–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15(8):1749–1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Dhingra, A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Ri AD, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury G, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C-E, Gutin A, Bumgarner R, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839. https://doiorg/10.1038/ng.654

    Google Scholar 

  • Vimolmangkang S, Han Y, Wei G, Korban SS (2013) An apple MYB transcription factor, MdMYB3, is involved in regulation of anthocyanin biosynthesis and flower development. BMC Plant Biol 13(1):176. https://doi.org/10.1186/1471-2229-13-176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Zhang S, Su L, Liu X, Hao Y (2013) A genome-wide analysis of the LBD (LATERAL ORGAN BOUNDARIES domain) gene family in Malus domestica with a functional characterization of MdLBD11. PLoS ONE 8(2):e57044. https://doi.org/10.1371/journal.pone.0057044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang R-K, Cao Z-H, Hao Y-J (2014) Overexpression of a R2R3 MYB gene MdSIMYB1 increases tolerance to multiple stresses in transgenic tobacco and apples. Physiol Plant 150(1):76–87

    Article  CAS  PubMed  Google Scholar 

  • Wang A, Tan D, Takahashi A, Zhong Li T, Harada T (2007) MdERFs, two ethylene-response factors involved in apple fruit ripening. J Exp Bot 58(13):3743–3748

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Xu H, Jiang S, Zhang Z, Lu N, Qiu H, Qu C, Wang Y, Wu S, Chen X (2017) MYB12 and MYB22 play essential roles in proanthocyanidin and flavonol synthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant J 90(2):276–292

    Google Scholar 

  • Wang F-P, Wang X-F, Zhang J, Ma F, Hao Y-J (2018a) MdMYB58 modulates Fe homeostasis by directly binding to the MdMATE43 promoter in plants. Plant Cell Physiol 59(12):2476–2489

    CAS  PubMed  Google Scholar 

  • Wang N, Qu C, Jiang S, Chen Z, Xu H, Fang H, Su M, Zhang J, Wang Y, Liu W, Zhang Z, Lu N, Chen X (2018b) The proanthocyanidin-specific transcription factor MdMYBPA1 initiates anthocyanin synthesis under low-temperature conditions in red-fleshed apples. Plant J 96(1):39–55

    Article  CAS  PubMed  Google Scholar 

  • Wang X-F, An J-P, Liu X, Su L, You C-X, Hao Y-J (2018c) The nitrate-responsive protein MdBT2 regulates anthocyanin biosynthesis by interacting with the MdMYB1 transcription factor. Plant Physiol 178(2):890–906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wang N, Xu H, Jiang S, Fang H, Zhang T, Su M, Xu L, Zhang Z, Chen X (2018d) Nitrogen affects anthocyanin biosynthesis by regulating MdLOB52 downstream of MdARF19 in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana). J Plant Growth Regul 37(3):719–729

    Google Scholar 

  • Wang Y, Liu W, Jiang H, Mao Z, Wang N, Jiang S, Xu H, Yang G, Zhang Z, Chen X (2019a) The R2R3-MYB transcription factor MdMYB24-like is involved in methyl jasmonate-induced anthocyanin biosynthesis in apple. Plant Physiol Biochem 139:273–282

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Li J, Mao Y, Zhang M, Wang R, Hu Y, Mao Z, Shen X (2019b) Transcriptional regulation of MdPIN3 and MdPIN10 by MdFLP during apple self-rooted stock adventitious root gravitropism. BMC Plant Biol 19(1):229. https://doi.org/10.1186/s12870-019-1847-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Sun J, Wang N, Xu H, Qu C, Jiang S, Fang H, Su M, Zhang Z, Chen X (2019c) MdMYBL2 helps regulate cytokinin-induced anthocyanin biosynthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana) callus. Funct Plant Biol 46(2):187–196

    Google Scholar 

  • Wang J-H, Gu K-D, Han P-L, Yu J-Q, Wang C-K, Zhang Q-Y, You C-X, Hu D-G, Hao Y-J (2020) Apple ethylene response factor MdERF11 confers resistance to fungal pathogen Botryosphaeria dothidea. Plant Sci 291:110351

    Article  CAS  PubMed  Google Scholar 

  • Wu R, Tomes S, Karunairetnam S, Tustin SD, Hellens RP, Allan AC, Macknight RC, Varkonyi-Gasic E (2017a) SVP-like MADS box genes control dormancy and budbreak in apple. Front Plant Sci 8:477. https://doi.org/10.3389/fpls.2017.00477

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu R, Wang Y, Wu T, Xu X, Han Z (2017b) MdMYB4, an R2R3-Type MYB transcription factor, plays a crucial role in cold and salt stress in apple calli. J Am Soc Hortic Sci 142(3):209–216

    Article  CAS  Google Scholar 

  • Xie X-B, Li S, Zhang R-F, Zhao J, Chen Y-C, Zhao Q, Yao Y-X, You C-X, Zhang X-S, Hao Y-J (2012) The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ 35(11):1884–1897

    Article  CAS  PubMed  Google Scholar 

  • Xie Y, Chen P, Yan Y, Bao C, Li X, Wang L, Shen X, Li H, Liu X, Niu C (2018) An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple. New Phytol 218(1):201–218

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Sun P, Jia F, Lu L, Li Y, Zhang S, Huang J (2014) Genomewide analysis of TCP transcription factor gene family in Malus domestica. J Genet 93(3):733–746

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Wang N, Liu J, Qu C, Wang Y, Jiang S, Lu N, Wang D, Zhang Z, Chen X (2017) The molecular mechanism underlying anthocyanin metabolism in apple using the MdMYB16 and MdbHLH33 genes. Plant Mol Biol 94(1–2):149–165

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Wang N, Wang Y, Jiang S, Fang H, Zhang J, Su M, Zuo W, Xu L, Zhang Z (2018a) Overexpression of the transcription factor MdbHLH33 increases cold tolerance of transgenic apple callus. Plant Cell Tiss Org Cult (PCTOC) 134(1):131–140

    Article  CAS  Google Scholar 

  • Xu H, Yang G, Zhang J, Wang Y, Zhang T, Wang N, Jiang S, Zhang Z, Chen X (2018b) Overexpression of a repressor MdMYB15L negatively regulates anthocyanin and cold tolerance in red-fleshed callus. Biochem Biophys Res Commun 500(2):405–410

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Liu X-D, Chi X-J, Wu C-A, Li Y-Z, Song L-L, Liu X-M, Wang Y-F, Wang F-W, Zhang C (2011) Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233(2):219–229

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Gao M, Huang L, Wang Y, van Nocker S, Wan R, Guo C, Wang X, Gao H (2017) Identification and expression analysis of the apple (Malus × domestica) basic helix-loop-helix transcription factor family. Sci Rep 7(1):1–14

    CAS  Google Scholar 

  • Yang Q, Chen Q, Zhu Y, Li T (2018) Identification of MdDof genes in apple and analysis of their response to biotic or abiotic stress. Funct Plant Biol 45(5):528–541

    Article  CAS  PubMed  Google Scholar 

  • Yang Y-Y, Ren Y-R, Zheng P-F, Qu F-J, Song L-Q, You C-X, Wang X-F, Hao Y-J (2020) Functional identification of apple MdMYB2 gene in phosphate-starvation response. J Plant Physiol 244:153089

    Article  CAS  PubMed  Google Scholar 

  • Yao J-L, Dong Y-H, Morris BA (2001) Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Natl Acad Sci 98(3):1306–1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yauk YK, Souleyre EJ, Matich AJ, Chen X, Wang MY, Plunkett B, Dare AP, Espley RV, Tomes S, Chagné D (2017) Alcohol acyl transferase 1 links two distinct volatile pathways that produce esters and phenylpropenes in apple fruit. Plant J 91(2):292–305

    Article  CAS  PubMed  Google Scholar 

  • Yin L, Wang Y, Yuan M, Zhang X, Xu X, Han Z (2014) Characterization of MxFIT, an iron deficiency induced transcriptional factor in Malus xiaojinensis. Plant Physiol Biochem 75:89–95

    Article  CAS  PubMed  Google Scholar 

  • Yue P, Lu Q, Liu Z, Lv T, Li X, Bu H, Liu W, Xu Y, Yuan H, Wang A (2020) Auxin-activated MdARF5 induces the expression of ethylene biosynthetic genes to initiate apple fruit ripening. New Phytol 226(6):1781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Li Y, Zhang Y, Wu C, Wang S, Hao L, Wang S, Li T (2017) Md-miR156ab and Md-miR395 target WRKY transcription factors to influence apple resistance to leaf spot disease. Front Plant Sci 8:526. https://doi.org/10.3389/fpls.2017.00526

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Xu H, Wang N, Jiang S, Fang H, Zhang Z, Yang G, Wang Y, Su M, Xu L (2018a) The ethylene response factor MdERF1B regulates anthocyanin and proanthocyanidin biosynthesis in apple. Plant Mol Biol 98(3):205–218

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Yuan L, Liu X, Chen X, Wang X (2018b) Evolution analysis of Dof transcription factor family and their expression in response to multiple abiotic stresses in Malus domestica. Gene 639:137–148

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Hu J, Han X, Li J, Gao Y, Richards CM, Zhang C, Tian Y, Liu G, Gul H (2019) A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nat Commun 10(1):1494. https://doi.org/10.1038/s41467-019-09518-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q-Y, Gu K-D, Cheng L, Wang J-H, Yu J-Q, Wang X-F, You C-X, Hu D-G, Hao Y-J (2020) BTB-TAZ domain protein MdBT2 modulates malate accumulation and vacuolar acidification in response to nitrate. Plant Physiol 183(2):750–764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao T, Liang D, Wang P, Liu J, Ma F (2012) Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Mol Genet Genomics 287(5):423–436

    Article  CAS  PubMed  Google Scholar 

  • Zhao Q, Ren Y-R, Wang Q-J, Yao Y-X, You C-X, Hao Y-J (2016) Overexpression of MdbHLH104 gene enhances the tolerance to iron deficiency in apple. Plant Biotechnol J 14(7):1633–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X-Y, Qi C-H, Jiang H, Zhong M-S, You C-X, Li Y-Y, Hao Y-J (2019a) MdHIR4 transcription and translation levels associated with disease in apple are regulated by MdWRKY31. Plant Mol Biol 101(1–2):149–162

    Article  CAS  PubMed  Google Scholar 

  • Zhao X-Y, Qi C-H, Jiang H, Zhong M-S, Zhao Q, You C-X, Li Y-Y, Hao Y-J (2019b) MdWRKY46-enhanced apple resistance to Botryosphaeria dothidea by activating the expression of MdPBS3.1 in the salicylic acid signaling pathway. Mol Plant Microbe Interact 32(10):1391–1401

    Google Scholar 

  • Zhao X-Y, Qi C-H, Jiang H, Zhong M-S, You C-X, Li Y-Y, Hao Y-J (2020) MdWRKY15 improves resistance of apple to Botryosphaeria dothidea via the salicylic acid-mediated pathway by directly binding the MdICS1 promoter. J Integr Plant Biol 62(4):527–543

    Article  CAS  PubMed  Google Scholar 

  • Zheng L, Ma J, Song C, Zhang L, Gao C, Zhang D, An N, Mao J, Han M (2018a) Genome-wide identification and expression analysis of GRF genes regulating apple tree architecture. Tree Genet Genomes 14(4):54. https://doi.org/10.1007/s11295-018-1267-8

    Article  Google Scholar 

  • Zheng X, Zhao Y, Shan D, Shi K, Wang L, Li Q, Wang N, Zhou J, Yao J, Xue Y (2018b) MdWRKY9 overexpression confers intensive dwarfing in the M26 rootstock of apple by directly inhibiting brassinosteroid synthetase MdDWF4 expression. New Phytol 217(3):1086–1098

    Article  CAS  PubMed  Google Scholar 

  • Zhou L-J, Li Y-Y, Zhang R-F, Zhang C-L, Xie X-B, Zhao C, Hao Y-J (2017a) The small ubiquitin-like modifier E3 ligase MdSIZ1 promotes anthocyanin accumulation by sumoylating MdMYB1 under low-temperature conditions in apple. Plant Cell Environ 40(10):2068–2080

    Article  CAS  PubMed  Google Scholar 

  • Zhou L-J, Mao K, Qiao Y, Jiang H, Li Y-Y, Hao Y-J (2017b) Functional identification of MdPIF1 as a phytochrome interacting factor in apple. Plant Physiol Biochem 119:178–188

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Biology, Shangdong Agricultural University, Shangdong, China

    Xiao-Fei Wang & Yu-Jin Hao

Authors
  1. Xiao-Fei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu-Jin Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiao-Fei Wang .

Editor information

Editors and Affiliations

  1. Department of Natural Resources and Environmental Sciences, University of Illinois at Urbana–Champaign, Urbana, IL, USA

    Schuyler S. Korban

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Wang, XF., Hao, YJ. (2021). Regulatory Sequences in Apple. In: Korban, S.S. (eds) The Apple Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-030-74682-7_9

Download citation

Publish with us

Policies and ethics

Search

Navigation