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Expression of MADS-box genes during the embryonic phase in Arabidopsis

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Abstract

MADS domain factors play important roles as developmental regulators in plants. In Arabidopsis thaliana, MADS domain proteins have been shown to regulate various processes during the vegetative and reproductive phases. Relatively little is known, however, about family members expressed during the embryonic phase and their function. To determine which MADS-box genes are expressed during the embryonic phase in Arabidopsis, a family-wide survey involving gene-specific primers and RT-PCR was conducted. Transcripts corresponding to 64 (out of 109 total) family members could be detected in RNA samples isolated from embryonic culture tissue. Eight MADS-box genes that appear to be expressed at higher levels during the embryonic phase than in seedlings or in inflorescence apices were identified. The spatial pattern of expression in developing seeds was characterized for four MADS-box genes (FLOWERING LOCUS C, FLOWERING LOCUS M, AGAMOUS-LIKE 15, and AGAMOUS-LIKE 18) using reporter constructs encoding translational fusions to GUS. All four are expressed in cells throughout the endosperm and embryo. Finally, to test the hypothesis that AGAMOUS-LIKE15 (AGL15) and AGAMOUS-LIKE18 (AGL18) play essential roles during the embryonic phase, plants carrying T-DNA insertions that disrupt these genes were isolated. No embryo defects were observed in agl15 or agl18 single mutants or in agl15agl18 double mutants. These results indicate that multiple regulatory pathways that involve MADS domain factors are likely to operate in embryonic tissues, and that genetic and/or functional redundancy are likely to be as prevalent as in other phases of the life cycle.

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Abbreviations

AGL:

AGAMOUS-like

BAC:

bacterial artificial chromosome

CTAB:

hexadecyl trimethyl-ammonium bromide

DIC:

differential interference contrast

ECT:

embryonic culture tissue

EF1α:

translation elongation factor

GM:

germination medium

GUS:

β-glucuronidase

MES:

2-(N-morpholino)ethanesulfonic acid

RT-PCR:

reverse transcriptase polymerase chain reaction

WS:

Wassilewskija

References

  • J.M. Alonso A. Stepanova T. Leisse C. Kim H. Chen P. Shinn D. Stevenson J. Zimmerman P. Barajas R. Cheuk C. Gadrinab C. Heller A. Jeske E. Koesema C. Meyers H. Parker L. Prednis Y. Ansari N. Choy H. Deen M. Geralt N. Hazari E. Hom M. Karnes C. Mulholland R. Ndubaku I. Schmidt P. Guzman L. Aguilar-Henonin M. Schmid D. Weigel D. Carter R. Marchand E. Risseeuw D. Brogden A. Zeko W. Crosby C. Berry J. Ecker (2003) ArticleTitleGenome-wide insertional mutagenesis of Arabidopsis thaliana Science 301 653–657

    Google Scholar 

  • E.R. Alvarez-Buylla S. Pelaz S.J. Liljegren S.E. Gold C. Burgeff G.S. Ditta L.R. Pouplana Particlede L. Martinez-Castilla M.F. Yanofsky (2000a) ArticleTitleAn ancestral MADS-box gene duplication occured before the divergence of plants and animals Proc. Natl. Acad. Sci. USA 97 5328–5333

    Google Scholar 

  • E.R. Alvarez-Buylla S.J. Liljegren S. Pelaz S.E. Gold C. Burgeff G.S. Ditta F. Vergara-Silva M.F. Yanofsky (2000b) ArticleTitleMADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes Plant J 24 457–466

    Google Scholar 

  • R. Amasino (2004) ArticleTitleVernalization, competence, and the epigenetic memory of winter Plant Cell 16 2553–2559

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • J.L. Bowman D.R. Smyth E.M. Meyerowitz (1991) ArticleTitleGenetic interactions among floral homeotic genes in Arabidopsis Development 112 1–20

    Google Scholar 

  • C. Burgeff S.J. Liljegren R. Tapia-López M.F. Yanofsky E.R. Alvarez-Buylla (2001) ArticleTitleMADS-box gene expression in lateral primordia, meristems and differentiated tissues of Arabidopsis thaliana roots Planta 214 365–372

    Google Scholar 

  • S. De Bodt J. Raes Y. Peer ParticleVan de G. Theißen (2003) ArticleTitleAnd then there were many: MADS goes genomic Trends Plant Sci 8 475–483

    Google Scholar 

  • M. Egea-Cortines H. Saedler H. Sommer (1999) ArticleTitleTernary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus EMBO J 18 5370–5379

    Google Scholar 

  • R. Favaro A. Pinyopich R. Battaglia M. Kooiker L. Borghi G. Ditta M.F. Yanofsky M.M. Kater L. Colombo (2003) ArticleTitleMADS-box protein complexes control carpel and ovule development in Arabidopsis Plant Cell 15 2603–2611

    Google Scholar 

  • D.E. Fernandez G.R. Heck S.E. Perry S.E. Patterson A.B. Bleecker S.-C. Fang (2000) ArticleTitleThe embryo MADS domain factor AGL15 acts postembryonically: inhibition of perianth senescence and abscission via constitutive expression Plant Cell 12 183–197

    Google Scholar 

  • C. Ferrándiz S.J. Liljegren M.F. Yanofsky (2000) ArticleTitleNegative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development Science 289 436–438

    Google Scholar 

  • M.K. Filipecki H. Sommer S. Malepszy (1997) ArticleTitleThe MADS-box CUS1 is expressed during cucumber somatic embryogenesis Plant Sci 125 63–74

    Google Scholar 

  • C.A. Flanagan H. Ma (1994) ArticleTitleSpatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant Arabidopsis flowers Plant Mol. Biol 26 581–595

    Google Scholar 

  • Q. Gu C. Ferrándiz M.F. Yanofsky R. Martienssen (1998) ArticleTitleThe FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development Development 125 1509–1517

    Google Scholar 

  • P. Hajdukiewicz Z. Svab P. Maliga (1994) ArticleTitleThe small, versatile pPZP family of Agrobacterium binary vectors for plant transformation Plant Mol. Biol 25 989–994

    Google Scholar 

  • E.W. Harding W. Tang K.W. Nichols D.E. Fernandez S.E. Perry (2003) ArticleTitleExpression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15 Plant Physiol 133 653–663

    Google Scholar 

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

    Google Scholar 

  • G.R. Heck S.E. Perry K.W. Nichols D.E. Fernandez (1995) ArticleTitleAGL15, a MADS domain protein expressed in developing embryos Plant Cell 7 1271–1282

    Google Scholar 

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

    Google Scholar 

  • S. Heuer S. Hansen J. Bantin R. Brettschneider E. Kranz H. Lörz T. Dresselhaus (2001) ArticleTitleThe maize MADS box gene ZmMADS3 affects node number and spikelet development and is co-expressed with ZmMADS1 during flower development, in egg cells, and early embryogenesis Plant Physiol 127 33–45

    Google Scholar 

  • T. Honma K. Goto (2001) ArticleTitleComplexes of MADS-box proteins are sufficient to convert leaves into floral organs Nature 409 525–529

    Google Scholar 

  • R.G. Immink TWJ Gadella SuffixJr. S. Ferrario M. Busscher G.C. Angenent (2002) ArticleTitleAnalysis of MADS box protein–protein interactions in living plant cells Proc. Natl. Acad. Sci. USA 99 2416–2421

    Google Scholar 

  • T. Jack (2001) ArticleTitlePlant development going MADS Plant Mol. Biol 46 515–520

    Google Scholar 

  • T. Kinoshita J.J. Harada R.B. Goldberg R.L. Fischer (2001) ArticleTitlePolycomb repression of flowering during early plant development Proc. Natl. Acad. Sci. USA 98 14156–14161

    Google Scholar 

  • R. Kofuji N. Sumikawa M. Yamasaki K. Kondo K. Ueda M. Ito M. Hasebe (2003) ArticleTitleEvolution and divergence of the MADS-box gene family based on genome-wide expression analyses Mol. Biol. Evol 20 1963–1977

    Google Scholar 

  • P.J. Krysan J.C. Young M.R. Sussman (1999) ArticleTitleT-DNA as an insertional mutagen in Arabidopsis Plant Cell 11 2283–2290

    Google Scholar 

  • C. Köhler L. Hennig C. Spillane S. Pien W. Gruissem U. Grossniklaus (2003) ArticleTitleThe Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1 Genes Dev 17 1540–1553

    Google Scholar 

  • H. Lee S.-S. Suh E. Park E. Cho J.H. Ahn S.-G. Kim J.S. Lee Y.M. Kwon I. Lee (2000) ArticleTitleThe AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis Genes Dev 14 2366–2376

    Google Scholar 

  • Lehti-Shiu, M. (2003). Characterization of MADS domain genes expressed during embryogenesis in Arabidopsis thaliana. Ph.D. thesis. University of Wisconsin-Madison

  • S.J. Liljegren G.S. Ditta Y. Eshed B. Savidge J.L. Bowman M.F. Yanofsky (2000) ArticleTitleSHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis Nature 404 766–770

    Google Scholar 

  • S.D. Michaels G. Ditta C. Gustafson-Brown S. Pelaz M. Yanofsky R.M. Amasino (2003) ArticleTitleAGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization Plant J 33 867–874

    Google Scholar 

  • S.D. Michaels R.M. Amasino (1999) ArticleTitleFlowering Locus C encodes a novel MADS domain protein that acts as a repressor of flowering Plant Cell 11 949–956

    Google Scholar 

  • T. Murashige F. Skoog (1962) ArticleTitleA revised medium for rapid growth and bioassays with tobacco tissue cultures Physiol. Plant 15 473–497

    Google Scholar 

  • M.G. Murray W.F. Thompson (1980) ArticleTitleRapid isolation of high molecular weight plant DNA Nucl. Acids Res 8 4321–4325

    Google Scholar 

  • J. Nam J. Kim S. Lee G. An H. Ma M. Nei (2004) ArticleTitleType 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

    Google Scholar 

  • N. Nesi I. Debeaujon C. Jond A.J. Stewart G.I. Jenkins M. Caboche L. Lepiniec (2002) ArticleTitleThe TRANSPARENT 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

    Google Scholar 

  • L. Parenicová Folter Sd. M. Kieffer D.S. Horner C. Favalli J. Busscher H.E. Cook R.M. Ingram M.M. Kater B. Davies G.C. Angenent L. Colombo (2003) ArticleTitleMolecular and phylognetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world Plant Cell 15 1538–1551

    Google Scholar 

  • S. Pelaz G.S. Ditta E. Baumann E. Wisman M.F. Yanofsky (2000) ArticleTitleB and C floral organ identity functions require SEPALLATA MADS-box genes Nature 405 200–203

    Google Scholar 

  • S.E. Perry K.W. Nichols D.E. Fernandez (1996) ArticleTitleThe MADS domain protein AGL15 localizes to the nucleus during early stages of seed development Plant Cell 8 1977–1989

    Google Scholar 

  • S.E. Perry H. Wang (2003) ArticleTitleRapid isolation of Arabidopsis thaliana developing embryos Biotechniques 35 278–282

    Google Scholar 

  • A. Pinyopich G.S. Ditta B. Savidge S.J. Liljegren E. Baumann E. Wisman M.F. Yanofsky (2003) ArticleTitleAssessing the redundancy of MADS-box genes during carpel and ovule development Nature 424 85–88

    Google Scholar 

  • M.D. Purugganan S.D. Rounsley R.J. Schmidt M.F. Yanofsky (1995) ArticleTitleMolecular evolution of flower development: diversification of the plant MADS-box regulatory gene family Genetics 140 345–356

    Google Scholar 

  • O.J. Ratcliffe G.C. Nadzan T.L. Reuber J.L. Riechmann (2001) ArticleTitleRegulation of flowering in Arabidopsis by an FLC homologue Plant Physiol 126 122–132

    Google Scholar 

  • O.J. Ratcliffe R.W. Kumimoto B.J. Wong J.L. Riechmann (2003) ArticleTitleAnalysis of the Arabidopsis MADS AFFECTING FLOWERING Gene Family: MAF2 prevents vernalization by short periods of cold Plant Cell 15 1159–1169

    Google Scholar 

  • J.L. Riechmann B.A. Krizek E.M. Meyerowitz (1996) ArticleTitleDimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS Proc. Natl. Acad. Sci. USA 93 4793–4798

    Google Scholar 

  • J.L. Riechmann E.M. Meyerowitz (1997) ArticleTitleMADS domain proteins in plant development Biol. Chem 378 1079–1101

    Google Scholar 

  • S.D. Rounsley G.S. Ditta M.F. Yanofsky (1995) ArticleTitleDiverse roles for MADS box genes in Arabidopsis development Plant Cell 7 1259–1269

    Google Scholar 

  • K.C. Scortecci S.D. Michaels R.M. Amasino (2001) ArticleTitleIdentification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering Plant J 26 229–236

    Google Scholar 

  • K.C. Scortecci S.D. Michaels R.M. Amasino (2003) ArticleTitleGenetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana Plant Mol. Biol 52 915–922

    Google Scholar 

  • P. Shore A.D. Sharrocks (1995) ArticleTitleThe MADS-box family of transcription factors Eur. J. Biochem 229 1–13

    Google Scholar 

  • H. Sommer J.-P Beltrán P. Huijser H. Pape W.-E Lönnig H. Saedler Z. Schwarz-Sommer (1990) ArticleTitleDeficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors EMBO J 9 605–613

    Google Scholar 

  • S. Sung R.M. Amasino (2004) ArticleTitleVernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3 Nature 427 159–164

    Google Scholar 

  • G. Theißen J.T. Kim H. Saedler (1996) ArticleTitleClassification 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

    Google Scholar 

  • H. Wang L.V. Caruso A.B. Downie S.E. Perry (2004) ArticleTitleThe embryo MADS domain protein AGAMOUS-Like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism Plant Cell 16 1206–1219

    Google Scholar 

  • H. Zhang B.G. Forde (1998) ArticleTitleAn Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture Science 279 407–409

    Google Scholar 

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Author notes

  1. Melissa D. Lehti-Shiu

    Present address: Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, IL, 60637, USA

Authors and Affiliations

  1. Department of Botany, University of Wisconsin-Madison, 430 Lincoln Drive, 53706, Madison, WI

    Melissa D. Lehti-Shiu, Benjamin J. Adamczyk & Donna E. Fernandez

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  1. Melissa D. Lehti-Shiu
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  2. Benjamin J. Adamczyk
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  3. Donna E. Fernandez
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Correspondence to Donna E. Fernandez.

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Lehti-Shiu, M.D., Adamczyk, B.J. & Fernandez, D.E. Expression of MADS-box genes during the embryonic phase in Arabidopsis. Plant Mol Biol 58, 89–107 (2005). https://doi.org/10.1007/s11103-005-4546-3

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