Skip to main content
SpringerLink
Log in

Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L.)

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

Abstract

MADS-box genes form a large family of transcription factors and play important roles in flower development and organ differentiation in plants. In this study, 42 wheat cDNAs encoding putative MADS-box genes were isolated. BLASTX searches and phylogenetic analysis indicated that the cDNAs represented 12 of the 14 MADS-box gene subfamilies. TaAGL14 and TaAGL15 formed a new subfamily along with a rice gene OsMADS32. RT-PCR analysis revealed that these genes had different exprsssion patterns in different organs of different stages. Expression patterns of TaAGL1 and TaAGL29 were also determined using in situ hybridization. TaAGL1 was abundantly expressed in primary root tips and the whole spikelet with more intense labeling at lodicules, paleas and stamens. TaAGL29 was expressed in both the non-reproductive parts (lemma, palea and glumes), and stamens and pistils. Moreover, differential expression patterns of these genes were also observed between wheat hybrid and its parents in leaf, stem and root of jointing stage, some were up-regulated while others were down-regulated in hybrid as compared to its parents. We concluded that multiple MADS-box genes exist in wheat genome and are expressed in tissue-specific patterns, and might play important roles in wheat growth and development.

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

References

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Angenent GC, Colombo L (1996) Molecular control of ovule development. Trends Plant Sci 1:228–232

    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  PubMed  CAS  Google Scholar 

  • Borner R, Kampmann G, Chandler J, Gleissner R, Wisman E, Apel K, Melzer S (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24:591–599

    Article  PubMed  CAS  Google Scholar 

  • Bove J, Jullien M, Grappin P (2002) Functional genomics in the study of seed germination. Genome Biol 3:1002–1010

    Google Scholar 

  • Cañas LA, Busscher M, Angenent GC, Beltran JP, Jvan Tunen AA (1994) Nuclear localization of the petunia MADS box genes protein FBP1. Plant J 6:597–604

    Article  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353(5):31–37

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ (1994) Evolution of a plant homeotic multigene family: towards connecting molecular systematics and molecular developmental genetics. Syst Biol 43:307–328

    Article  Google Scholar 

  • Fu D, Szucs P, Yan L, Helguera M, Skinner JS, von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Genet Genomics 273(1):54–65

    Article  PubMed  CAS  Google Scholar 

  • Gu Q, Ferrandiz C, Yanofsky MF, Martienssen R (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125:1509–1517

    PubMed  CAS  Google Scholar 

  • Hama E, Takumi S, Ogihara Y, Murai K (2004) Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218:712–720

    Article  PubMed  CAS  Google Scholar 

  • Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360

    Article  PubMed  CAS  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 19:801–814

    PubMed  CAS  Google Scholar 

  • Himi E, Noda K (2004) Isolation and location of three homoeoogous dihydroflavonol-4-reductase (DFR) genes of wheat and their tissue-dependent expression. J Exp Bot 55:365–375

    Article  PubMed  CAS  Google Scholar 

  • Kane NA, Danyluk J, Tardif G, Ouellet F, Laliberte JF, Limin AE, Fowler DB, Sarhan F (2005) TaVRT-2, a member of the StMADS-11 clade of flowering repressors, is regulated by vernalization and photoperiod in wheat. Plant Physiol 138(4):2354–2363

    Article  PubMed  CAS  Google Scholar 

  • Kang HG, Noh YS, Chung YY, Costa MA, An K, An G (1995) Phenotypic alterations of petal and sepal by ectopic expression of a rice MADS box gene in tobacco. Plant Mol Biol 29:1–10

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann K, Freialdenhoven A, Vincent C, Li MA, Saedler H, Theißen G (2002) A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Mol Genet Genomics 266:942–950

    Article  PubMed  CAS  Google Scholar 

  • Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267:522–525

    Article  PubMed  CAS  Google Scholar 

  • Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14:2366–2376

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Kim J, Han JJ, Han MJ, An G (2004) Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in rice. Plant J 38(5):754–764

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Dee ZP, Wittich P, Pe ME, Rigola D, Del Buono I, Sari Gorla M, Kater MM, Colombo L (1999) OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev Genet 25:237–244

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Yanofsky MF, Meyerowitz EM (1991) AGL1–AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5:484–495

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Yanofsky MF (1998) The Arabidopsis AGL9 MADS box gene is expressed in young flower primordial. Sex Plant Reprod 11:22–28

    Article  CAS  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277

    Article  PubMed  CAS  Google Scholar 

  • Meguro A, Takumi S, Ogihara Y, Murai K (2003) WAG, a wheat AGAMOUS homolog, is associated with development of pistillike stamens in alloplasmic wheats. Sex Plant Reprod 15:221–230

    CAS  Google Scholar 

  • Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623

    Article  PubMed  CAS  Google Scholar 

  • Münster T, Deleu W, Wingen LU, Ouzunova M, Cacharrón J, Faigl W, Werth S, Kim JTT, Saedler H, Theißen G (2002) Maize MADS-box genes galore. Maydica 47:287–301

    Google Scholar 

  • Murai K, Murai R, Takumi S, Ogihara Y (1998) Cloning and characterization of cDNAs corresponding to the wheat MADS-box genes. In: Slinkard AE (ed) Proceedings of the 9th international wheat genet symposium. University Extension Press, Sasketchewan, pp 89–94

  • Murai K, Takumi S, Koga H, Ogihara Y (2002) Pistillody, homeotic transformation of stamens into pistil-like structures, caused by nuclear-cytoplasm interaction in wheat. Plant J 29:169–181

    Article  PubMed  Google Scholar 

  • Murai K, Miyama ME, Kato H, Takumi S, Ogihara Y (2003) WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol 44:1255–1265

    Article  PubMed  CAS  Google Scholar 

  • Nam J, Kim J, Lee S, An G, Ma H, Nei M (2004) Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms. Proc Natl Acad Sci USA 101:1910–1915

    Article  PubMed  CAS  Google Scholar 

  • Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L (2002) The TRANSPARANT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14:2463–2479

    Article  PubMed  CAS  Google Scholar 

  • Ng M, Yanofsky MF (2001) Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell 13(4):739–753

    Article  PubMed  CAS  Google Scholar 

  • Ni ZF, Sun QX, Wu LM, Xie CJ (2002) Differential gene expression between wheat hybrids and their parental inbreds in primary roots. Acta Bot Sin 44:457–462

    CAS  Google Scholar 

  • Nomura T, Ishihara A, Yanagita RC, Endo TR, Iwamura H (2005) Three genomes differentially contribute to the biosynthesis of benzoxazinones in hexaplois wheat. Proc Natl Acad Sci USA 102:16490–16495

    Article  PubMed  CAS  Google Scholar 

  • Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15(7):1538–1551

    Article  PubMed  CAS  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    Article  PubMed  CAS  Google Scholar 

  • Pelucchi N, Fornara F, Favalli C, Masiero S, Lago C, Pe E, Colombo L, Kater MM (2002) Comparative analysis of rice MADS-box genes expressed during flower development. Sex Plant Reprod 15:113–122

    Article  CAS  Google Scholar 

  • Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995a) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140:345–356

    CAS  Google Scholar 

  • Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995b) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140(1):345–356

    CAS  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378(10):1079–1101

    Article  PubMed  CAS  Google Scholar 

  • Rounsley SD, Ditta GS, Yanofsky MF (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7:1259–1269

    Article  PubMed  CAS  Google Scholar 

  • Schmitz J, Franzen R, Ngyuen 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(6):899–913

    Article  PubMed  CAS  Google Scholar 

  • Shore P, Sharrocks AD (1995) The MADS-box family of transcription factors. Eur J Biochem 229:1–13

    Article  PubMed  CAS  Google Scholar 

  • Sun QX, Wu LM, Ni ZF (2004) Differential gene expression patterns in leaves between hybrids and their parental inbreds are correlated with heterosis in a wheat diallel cross. Plant Sci 166:651–657

    Article  CAS  Google Scholar 

  • Theißen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4(1):75–85

    Article  PubMed  Google Scholar 

  • Theißen G, Saedler H (1995) MADS-box genes in plant ontogeny and phylogeny: Haeckel’s ‘biogenetic law’ revisited. Curr Opin Genet Dev 5:628–639

    Article  PubMed  Google Scholar 

  • Theißen G, Saedler H (1999) The golden decade of molecular floral development (1990–1999): a cheerful obituary. Dev Genet 25(3):181–193

    PubMed  Google Scholar 

  • Theißen G, Saedler H (2001) Plant biology. Floral quartets. Nature 409(6819):469–471

    Article  PubMed  Google Scholar 

  • 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 43:484–516

    Article  PubMed  Google Scholar 

  • Theißen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149

    Article  PubMed  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78(2):203–209

    Article  PubMed  CAS  Google Scholar 

  • West AG, Causier BE, Davies B, Sharrocks AD (1998) DNA binding and dimerisation determinants of Antirrhinum majus MADS-box transcription factors. Nucleic Acids Res 26:5277–5287

    Article  PubMed  CAS  Google Scholar 

  • Wu LM, Ni ZF, Meng FR, Lin Z, Sun QX (2003) Cloning and characterization of leaf cDNAs that are differentially expressed between wheat hybrids and their parents. Mol Genet Genomics 270:281–286

    Article  PubMed  CAS  Google Scholar 

  • Yanofsky M, Ma H, Bowman G, Drews K, Feldmann K, Meyerowitz E (1990) The protein encoded by the Arabidodpsis homeotic gene AGAMOUS resembles transcriptional factors. Nature 346:35–39

    Article  PubMed  CAS  Google Scholar 

  • Yao YY, Ni ZF, Zhang YH, Chen Y, Ding YH, Han ZF, Liu ZY, Sun QX (2005) Identification of differentially expressed genes in leaf and root between wheat hybrid and its parental inbreds using PCR-based cDNA subtraction. Plant Mol Biol 58:367–384

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409

    Article  PubMed  CAS  Google Scholar 

  • Zhao YX, Cheng ZJ, Zhang XS (2005) Overexpression of TaMADS1, a SEPALLATA-like gene in wheat, causes early flowering and the abnormal development of floral organs in Arabidopsis. Planta 22:1–10

    Google Scholar 

Download references

Acknowledgments

This work was financially supported by the State Key Basic Research and Development Plan of China (2001CB1088), National Science Found for Distinguished Young Scholars (39925026) and National Natural Science Foundation of China (30000109, 30270824).

Author information

Authors and Affiliations

  1. Department of Plant Genetics and Breeding, State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing, China

    Tao Zhao, Zhongfu Ni, Yan Dai, Yingyin Yao, Xiuling Nie & Qixin Sun

  2. Key Laboratory of Crop Heterosis and Utilization, Ministry of Education, Beijing, China

    Tao Zhao, Zhongfu Ni, Yan Dai, Yingyin Yao, Xiuling Nie & Qixin Sun

  3. Key Laboratory of Crop Genomics and Genetic Improvement, Ministry of Agriculture, Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing, 100094, China

    Tao Zhao, Zhongfu Ni, Yan Dai, Yingyin Yao, Xiuling Nie & Qixin Sun

Authors
  1. Tao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhongfu Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yingyin Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiuling Nie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qixin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qixin Sun.

Additional information

Communicated by J.-K. Zhu

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, T., Ni, Z., Dai, Y. et al. Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L.). Mol Genet Genomics 276, 334–350 (2006). https://doi.org/10.1007/s00438-006-0147-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-006-0147-3

Keywords

Search

Navigation