Plant Molecular Biology Reporter

, Volume 37, Issue 1–2, pp 24–40 | Cite as

Homotypic Clusters of Transcription Factor Binding Sites in the First Large Intron of AGL24 MADS-Box Transcription Factor Are Recruited in the Enhancement of Floral Expression

  • Tajammul Hussain
  • Nazia Rehman
  • Safeena Inam
  • Wajya Ajmal
  • Amber Afroz
  • Aish Muhammad
  • Yusuf Zafar
  • Ghulam Muhammad Ali
  • Muhammad Ramzan KhanEmail author
Original Article


The occurrence of homotypic clusters of transcription factor binding sites (HCTs) and their contribution to regulatory evolution is documented in animals, but their manifestation in regulating plant genome expression remained an enigma. To explore the existence and functions of HCTs in highly constrained non-coding sequences of MADS-box transcription factors—generally involved in floral organ identity and phase transition—we employed cis-regulatory cluster finding in silico tools augmented with in vitro assays and site-directed mutagenesis in the STMADS11 superclade of this family. Thousands of transcription factor binding sites (TFBSs) organized into HCTs and multiple-factor binding elements belonging to various families of TFs were identified in the promoter as well as in the intronic region of the selected members of STMADS11 subfamily. A total of 151 HCTs were detectable in the defined promoter in comparison with 144 in the intronic regions. The MADS-domain binding HCTs (overlapping CArG-boxes) constitute a major portion (18%) of these HCTs. A protrusive HCT of 11 TFBSs was identified in the 1st large intron of the AGAMOUS LIKE 24 (AGL24) pertinent to the SVP clade of the STMADS11 subfamily but no such cluster could be detected in the region proximal to the core promoter. These HCTs in the intronic region could bind the SEP4 MADS-domain protein as revealed by in vitro assay. Using HCT cluster swapping of CArG-boxes through the GUS reporter assay, it was possible to empirically validate that a change in the position of intronic MADS-box cluster of AGL24 to the promoter region adjacent to the transcriptional start site (TSS) invoke an enhancement of floral expression. This study unveils the occurrence of HCTs in both the promoter and downstream intronic regions in the selected members of the STMADS11 subfamily of plants. These HCTs play an important role in deciphering the gene regulatory code of MADS-box TFs particularly AGL24.


HCTs CRMs MADS-box CArG-box AGL24 Arabidopsis Expression Regulatory elements Promoter 



We thank Drs. Amir Ali Abbasi (NCB, QAU, Islamabad, Pakistan) for valuable discussions and comments. Sincere appreciation and gratitude to the anonymous reviewers for valuable comments and suggestions that help improve the quality and language of this manuscript.

Authors’ contribution

MRK conceived and designed the experiments. TH, NR, SI, WA, AA, AM, GMA, and MRK carried out the experiments. MRK and TH drafted the manuscript. MRK, WA, and YZ edited the manuscript. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Competing Interests

The authors declare that there are no competing interests.

Supplementary material

11105_2019_1136_MOESM1_ESM.docx (45 kb)
ESM 1 (DOCX 44 kb)


  1. Abbasi AA, Minhas R, Schmidt A, Koch S, Grzeschik KH (2013) Cis-regulatory underpinnings of human GLI3 expression in embryonic craniofacial structures and internal organs. Develop Growth Differ 55:699–709CrossRefGoogle Scholar
  2. Alter P, Bircheneder S, Zhou LZ, Schlüter U, Gahrtz M, Sonnewald U, Dresselhaus T (2016) Flowering time regulated genes in maize include the transcription factor ZmMADS1. Plant Physiol 172:389–404CrossRefPubMedPubMedCentralGoogle Scholar
  3. Barah P, B N MN, Jayavelu ND, Sowdhamini R, Shameer K, Bones AM (2016) Transcriptional regulatory networks in Arabidopsis thaliana during single and combined stresses. Nucleic Acids Res 44:3147–3164CrossRefPubMedGoogle Scholar
  4. 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 29:464–489CrossRefPubMedGoogle Scholar
  5. Cheng L, Wenlong S, Xiaoxia W, Caiyun Y, Zhe S, Jinhui F (2015) Antisense expression of PtMADS1 gene from Populus tomentosa. Molecular Plant Breeding 02:792.117Google Scholar
  6. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  7. Cohen O, Borovsky Y, David-Schwartz R, Paran I (2012) CaJOINTLESS is a MADS-box gene involved in suppression of vegetative growth in all shoot meristems in pepper. J Exp Bot 63:4947–4957CrossRefPubMedPubMedCentralGoogle Scholar
  8. Crocker J, Potter N, Erives A (2010) Dynamic evolution of precise regulatory encodings creates the clustered site signature of enhancers. Nat Commun 1:99CrossRefPubMedPubMedCentralGoogle Scholar
  9. Davies B, Motte P, Keck E, Saedler H, Sommer H, Schwarz-Sommer Z (1999) PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J 18:4023–4034CrossRefPubMedPubMedCentralGoogle Scholar
  10. De Folter S, Immink RG, Kieffer M, Pařenicová L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17:1424–1433CrossRefPubMedPubMedCentralGoogle Scholar
  11. De Folter S, Shchennikova AV, Franken J, Busscher M, Baskar R, Grossniklaus U, Angenent GC, Immink RG (2006) A Bsister MADS-box gene involved in ovule and seed development in petunia and Arabidopsis. Plant J 47:934–946CrossRefPubMedGoogle Scholar
  12. De Folter S, Urbanus SL, van Zuijlen LG, Kaufmann K, Angenent GC (2007) Tagging of MADS domain proteins for chromatin immunoprecipitation. BMC Plant Biol 7:47CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940CrossRefPubMedGoogle Scholar
  14. Doyle JJ (1994) Evolution of a plant homeotic multigene family: toward connecting molecular systematics and molecular developmental genetics. Syst Biol 43:307–328Google Scholar
  15. Espinosa-Soto C, Padilla-Longoria P, Alvarez-Buylla ER (2004) A gene regulatory network model for cell-fate determination during Arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles. Plant Cell 16:2923–2939CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ferrario S, Immink RG, Shchennikova A, Busscher-Lange J, Angenent GC (2003) The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell 15:914–925CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fornara F, Gregis V, Pelucchi N, Colombo L, Kater MM (2008) The rice StMADS11-like genes OsMADS22 and OsMADS47 cause floral reversions in Arabidopsis without complementing the svp and agl24 mutants. J Exp Bot 59:2181–2190CrossRefPubMedPubMedCentralGoogle Scholar
  18. Garcia-Maroto F, Ortega N, Lozano R, Carmona M (2000) Characterization of the potato MADS-box gene STMADS16 and expression analysis in tobacco transgenic plants. Plant Mol Biol 42:499–513CrossRefPubMedGoogle Scholar
  19. Gómez-Mena C, de Folter S, Costa MMR, Angenent GC, Sablowski R (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132:429–438CrossRefPubMedGoogle Scholar
  20. Gotea V, Visel A, Westlund JM, Nobrega MA, Pennacchio LA, Ovcharenko I (2010) Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res 20:565–577CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gramzow L, Theissen G (2010) A hitchhiker's guide to the MADS world of plants. Genome Biol 11:214CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gramzow L, Theißen G (2015) Phylogenomics reveals surprising sets of essential and dispensable clades of MIKCc-group MADS-box genes in flowering plants. J Exp Zool B Mol Dev Evol 324:353–362CrossRefPubMedGoogle Scholar
  23. Gramzow L, Weilandt L, Theißen G (2014) MADS goes genomic in conifers: towards determining the ancestral set of MADS-box genes in seed plants. Ann Bot 114:1407–1429CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gregis V, Sessa A, Colombo L, Kater MM (2008) AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. Plant J 56:891–902CrossRefPubMedGoogle Scholar
  25. Gregis V, Sessa A, Dorca-Fornell C, Kater MM (2009) The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes. Plant J 60:626–637CrossRefPubMedGoogle Scholar
  26. Gregis V, Andrés F, Sessa A, Guerra RF, Simonini S, Mateos JL, Torti S, Zambelli F, Prazzoli GM, Bjerkan KN, Grini PE, Pavesi G, Colombo L, Coupland G, Kater MM (2013) Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during vegetative and reproductive development in Arabidopsis. Genome Biol 14:R56CrossRefPubMedPubMedCentralGoogle Scholar
  27. Han A, Pan F, Stroud JC, Youn HD, Liu JO, Chen L (2003) Sequence-specific recruitment of transcriptional co-repressor Cabin1 by myocyte enhancer factor-2. Nature 422:730–734CrossRefPubMedGoogle Scholar
  28. Hardison RC, Taylor J (2012) Genomic approaches to finding cis-regulatory modules in animals. Nat Rev Gene 13:469–483CrossRefGoogle Scholar
  29. Hartmann U, Höhmann S, Nettesheim K, Wisman E, Saedler H (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360CrossRefPubMedGoogle Scholar
  30. He C, Saedler H (2005) Heterotopic expression of MPF2 is the key to the evolution of the Chinese lantern of Physalis, a morphological novelty in Solanaceae. Proc Natl Acad Sci U S A 102:5779–5784CrossRefPubMedPubMedCentralGoogle Scholar
  31. He C, Tian Y, Saedler R, Efremova N, Riss S, Khan MR, Yephremov A, Saedler H (2010) The MADS-domain protein MPF1 of Physalis floridana controls plant architecture, seed development and flowering time. Planta 231:767–777CrossRefPubMedGoogle Scholar
  32. Heuer S, Lörz H, Dresselhaus TR (2000) The MADS box gene ZmMADS 2 is specifically expressed in maize pollen and during maize pollen tube growth. Sex Plant Reprod 13:21–27CrossRefGoogle Scholar
  33. Hu J-Y, Saedler H (2007) Evolution of the inflated calyx syndrome in Solanaceae. Mol Bio Evol 24:2443–2453CrossRefGoogle Scholar
  34. Jetha K, Theißen G, Melzer R (2014) Arabidopsis SEPALLATA proteins differ in cooperative DNA-binding during the formation of floral quartet-like complexes. Nucleic Acids Res 42:10927–10942CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kane NA, Agharbaoui Z, Diallo AO, Adam H, Tominaga Y, Ouellet F, Sarhan F (2007) TaVRT2 represses transcription of the wheat vernalization gene TaVRN1. Plant J 51:670–680CrossRefPubMedGoogle Scholar
  36. Kaufmann K, Muino JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7:e1000090CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kaufmann K, Wellmer F, Muiño JM, Ferrier T, Wuest SE, Serrano-Mislata A, Madueño F, Krajewski P, Meyerowitz EM, Angenent GC, Riechmann JL (2010) Orchestration of floral initiation by APETALA1. Science 328:85–89CrossRefPubMedGoogle Scholar
  38. Khan MR, Ali GM (2013) Functional evolution of cis-regulatory modules of STMADS11 superclade MADS-box genes. Plant Mol Biol 83:489–506CrossRefPubMedGoogle Scholar
  39. Khan MR, Hu J-Y, Riss S, He C, Saedler H (2009) MPF2-like-A MADS-box genes control the inflated calyx syndrome in Withania (Solanaceae): roles of Darwinian selection. Mol Biol Evol 26:2463–2473CrossRefPubMedGoogle Scholar
  40. Khan MR, Hu J, Ali GM (2012) Reciprocal loss of CArG-boxes and auxin response elements drives expression divergence of MPF2-like MADS-box genes controlling calyx inflation. PLoS One 7:e42781CrossRefPubMedPubMedCentralGoogle Scholar
  41. Khan MR, Khan IU, Ali GM (2013) MPF2-like MADS-box genes affecting expression of SOC1 and MAF1 are recruited to control flowering time. Mol Biotechnol 54:25–36CrossRefPubMedGoogle Scholar
  42. Kim S-H, Mizuno K, Fujimura T (2002) Isolation of MADS-box genes from sweet potato (Ipomoea batatas (L.) Lam.) expressed specifically in vegetative tissues. Plant and. Cell Physiol 43:314–322CrossRefGoogle Scholar
  43. Kooiker M, Airoldi CA, Losa A, Manzotti PS, Finzi L, Kater MM, Colombo L (2005) BASIC PENTACYSTEINE1, a GA binding protein that induces conformational changes in the regulatory region of the homeotic Arabidopsis gene SEEDSTICK. Plant Cell 17:722–729CrossRefPubMedPubMedCentralGoogle Scholar
  44. Lee S, Kim J, Son JS, Nam J, Jeong DH, Lee K, Jang S, Yoo J, Lee J, Lee DY, Kang HG, An G (2003) Systematic reverse genetic screening of T-DNA tagged genes in rice for functional genomic analyses: MADS-box genes as a test case. Plant Cell Physiol 44:1403–1411CrossRefPubMedGoogle Scholar
  45. Lee S, Choi SC, An G (2008) Rice SVP-group MADS-box proteins, OsMADS22 and OsMADS55, are negative regulators of brassinosteroid responses. Plant J 54:93–105CrossRefPubMedGoogle Scholar
  46. Li ZM, Zhang JZ, Mei L, Deng XX, Hu CG, Yao JL (2010) PtSVP, an SVP homolog from trifoliate orange (Poncirus trifoliata L. Raf.), shows seasonal periodicity of meristem determination and affects flower development in transgenic Arabidopsis and tobacco plants. Plant Mol Biol 74:129–142CrossRefPubMedGoogle Scholar
  47. Li Q, Byrns B, Badawi MA, Diallo AB, Danyluk J, Sarhan F, Laudencia-Chingcuanco D, Zou J, Fowler DB (2018) Transcriptomic insights into phenological development and cold tolerance of wheat grown in the field. Plant Physiol 176:2376–2394CrossRefGoogle Scholar
  48. Lifanov AP, Makeev VJ, Nazina AG, Papatsenko DA (2003) Homotypic regulatory clusters in Drosophila. Genome Res 13:579–588CrossRefPubMedPubMedCentralGoogle Scholar
  49. Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770CrossRefPubMedGoogle Scholar
  50. Liu C, Zhou J, Bracha-Drori K, Yalovsky S, Ito T, Yu H (2007) Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development 134:1901–1910CrossRefPubMedGoogle Scholar
  51. Loots GG, Ovcharenko I (2004) rVISTA 2.0: evolutionary analysis of transcription factor binding sites. Nucleic Acids Res 32:217–221CrossRefGoogle Scholar
  52. Mantegazza O, Gregis V, Chiara M, Selva C, Leo G, Horner DSKMM (2014) Gene coexpression patterns during early development of the native Arabidopsis reproductive meristem: novel candidate developmental regulators and patterns of functional redundancy. Plant J Cell Mol Biol 79:861–877CrossRefGoogle Scholar
  53. Mao L, Begum D, H-w C, Budiman MA, Szymkowiak EJ (2000) JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature 406:910–913CrossRefPubMedGoogle Scholar
  54. Matys V, Fricke E, Geffers R, Gössling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, Kloos DU, Land S, Lewicki-Potapov B, Michael H, Münch R, Reuter I, Rotert S, Saxel H, Scheer M, Thiele S, Wingender E (2003) TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31:374–378CrossRefPubMedPubMedCentralGoogle Scholar
  55. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956CrossRefPubMedPubMedCentralGoogle Scholar
  56. Michaels SD, Ditta G, Gustafson-Brown C, Pelaz S, Yanofsky M, Amasino RM (2003) AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J 33:867–874CrossRefPubMedGoogle Scholar
  57. O’Malley RC, Huang S-s C, Song L, Galli M, Gallavotti A, Ecker JR (2016) Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 165:1280–1292CrossRefPubMedPubMedCentralGoogle Scholar
  58. Ovcharenko I, Loots GG, Giardine BM, Hou M, Ma J, Hardison RC, Stubbs L, Miller W (2005) Mulan: multiple-sequence local alignment and visualization for studying function and evolution. Genome Res 15:184–194CrossRefPubMedPubMedCentralGoogle Scholar
  59. Pennacchio LA, Bickmore W, Dean A, Nobrega MA, Bejerano G (2013) Enhancers: five essential questions. Nat Rev Gene 14:288–295CrossRefGoogle Scholar
  60. Pollock R, Treisman R (1991) Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev 5:2327–2341CrossRefPubMedGoogle Scholar
  61. Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140:345–356PubMedPubMedCentralGoogle Scholar
  62. Ramamoorthy R, Phua EE-K, Lim S-H, Tan HT-W, Kumar PP (2013) Identification and characterization of RcMADS1, an AGL24 ortholog from the holoparasitic plant Rafflesia cantleyi Solms-Laubach (Rafflesiaceae). PLoS One 8(6):e67243CrossRefPubMedPubMedCentralGoogle Scholar
  63. Riechmann JL, Krizek BA, Meyerowitz EM (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci U S A 93:4793–4798CrossRefPubMedPubMedCentralGoogle Scholar
  64. Schmitz J, Franzen R, Nguyen TH, Garcia-Maroto F, Pozzi C, Salamini F, Rohde W (2000) Cloning, mapping and expression analysis of barley MADS-box genes. Plant Mol Biol 42:899–913CrossRefPubMedGoogle Scholar
  65. Schmitz JF, Zimmer F, Bornberg-Bauer E (2016) Mechanisms of transcription factor evolution in Metazoa. Nucleic Acids Res 44:6287–6297CrossRefPubMedPubMedCentralGoogle Scholar
  66. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931–936CrossRefPubMedGoogle Scholar
  67. Sentoku N, Kato H, Kitano H, Imai R (2005) OsMADS22, an STMADS11-like MADS-box gene of rice, is expressed in non-vegetative tissues and its ectopic expression induces spikelet meristem indeterminacy. Mol Gen Genomics 273:1–9CrossRefGoogle Scholar
  68. Shlyueva D, Stelzer C, Gerlach D, Yáñez-Cuna JO, Rath M, Boryn LM, Arnold CD, Stark A (2014) Hormone-responsive enhancer-activity maps reveal predictive motifs, indirect repression, and targeting of closed chromatin. Mol Cell 54:180–192CrossRefPubMedGoogle Scholar
  69. Shore P, Sharrocks AD (1995) The MADS-box family of transcription factors. The FEBS J 229:1–13Google Scholar
  70. Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9:355–365CrossRefPubMedPubMedCentralGoogle Scholar
  71. Sussmilch FC, Hecht V, Vander Schoor JK, Weller JL (2017) Identification of the SHORT VEGETATIVE PHASE (SVP)-like MADS-box genes in pea (Pisum sativum L.). Plant Gene 12:72–79CrossRefGoogle Scholar
  72. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  73. Tang W, Perry SE (2003) Binding site selection for the plant MADS domain protein AGL15 an in vitro and in vivo study. J Biol Chem 278:28154–28159CrossRefPubMedGoogle Scholar
  74. Theissen G, Strater T, Fischer A, Saedler H (1995) Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of AGAMOUS-like MADS-box genes from maize. Gene 156:155–166CrossRefPubMedGoogle Scholar
  75. Theißen G, Kim JT, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43:484–516CrossRefPubMedGoogle Scholar
  76. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149CrossRefPubMedGoogle Scholar
  77. Thouet J, Quinet M, Lutts S, Kinet JM, Périlleux C (2012) Repression of floral meristem fate is crucial in shaping tomato inflorescence. PLoS One 7:e31096CrossRefPubMedPubMedCentralGoogle Scholar
  78. Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357CrossRefPubMedGoogle Scholar
  79. Van Mourik S, van Dijk AD, de Gee M, Immink RG, Kaufmann K, Angenent GC, van Ham RC, Molenaar J (2010) Continuous-time modeling of cell fate determination in Arabidopsis flowers. BMC Syst Biol 4: 101Google Scholar
  80. Wang YQ, Melzer R, Theißen G (2010) Molecular interactions of orthologues of floral homeotic proteins from the gymnosperm Gnetum gnemon provide a clue to the evolutionary origin of ‘floral quartets. Plant J 64:177–190CrossRefPubMedGoogle Scholar
  81. West AG, Shore P, Sharrocks AD (1997) DNA binding by MADS-box transcription factors: a molecular mechanism for differential DNA bending. Mol Cell Biol 17(5):2876–2887CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wu R, Tomes S, Karunairetnam S, Tustin SD, Hellens RP, Allan AC, Macknight RC, Varkonyi-Gasic E (2017) SVP-like MADS box genes control dormancy and budbreak in apple. Front Plant Sci 8, 477Google Scholar
  83. Yu H, Xu Y, Tan EL, Kumar PP (2002) AGAMOUS-LIKE 24, a dosage-dependent mediator of flowering signals. Proc Natl Acad Sci U S A 99:16336–16341CrossRefPubMedPubMedCentralGoogle Scholar
  84. Yu H, Ito T, Wellmer F, Meyerowitz EM (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet 36: 157–161Google Scholar
  85. Zhang J, Khan MR, Tian Y, Li Z, Riss S, He C (2012) Divergences of MPF2-like MADS-domain proteins have an association with the evolution of the inflated calyx syndrome within Solanaceae. Planta 236:1247–1260CrossRefPubMedGoogle Scholar
  86. Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21:2563–2577CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Tajammul Hussain
    • 1
    • 2
  • Nazia Rehman
    • 1
  • Safeena Inam
    • 1
  • Wajya Ajmal
    • 1
  • Amber Afroz
    • 3
  • Aish Muhammad
    • 1
  • Yusuf Zafar
    • 4
  • Ghulam Muhammad Ali
    • 1
  • Muhammad Ramzan Khan
    • 1
    • 5
    Email author
  1. 1.National Institute for Genomics and Advanced Biotechnology (NIGAB)National Agricultural Research CentreIslamabadPakistan
  2. 2.Faculty of Biochemical and Chemical EngineeringTechnical University DortmundDortmundGermany
  3. 3.Department of Biochemistry and Molecular BiologyUniversity of GujratGujratPakistan
  4. 4.Pakistan Agricultural Research CouncilIslamabadPakistan
  5. 5.National Centre for BioinformaticsQuaid-i-Azam UniversityIslamabadPakistan

Personalised recommendations