Advertisement
JOURNAL ARTICLES
SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein
M.G. Heisler, A. Atkinson, Y.H. Bylstra, R. Walsh, D.R. Smyth
Development 2001 128: 1089-1098;

Summary

Studies involving mutants of the gene SPATULA indicate that it promotes the growth of carpel margins and of pollen tract tissues derived from them. We show that it encodes a new member of the basic-helix-loop-helix family of transcription factors. SPATULA is expressed in marginal and pollen tract tissues throughout their development confirming its role in regulating their growth. It is also expressed in many other tissues where it may act redundantly to control growth, including the peripheral zone of the shoot apical meristem, and specific tissues within leaves, petals, stamens and roots. Expression in the stomium, funiculus and valve dehiscence zone indicates an additional role in abscission. SPATULA expression does not require the function of the other carpel development genes CRABS CLAW and AGAMOUS, although its expression is repressed in first whorl organs by the A function gene APETALA2. Further, we have shown that disruptions to gynoecial pattern formation seen in ettin mutants can largely be attributed to ectopic SPATULA action. ETTIN's role seems to be to negatively regulate SPATULA expression in abaxial regions of the developing gynoecium. SPATULA is the first basic-helix-loop-helix gene in plants known to play a role in floral organogenesis.

Reference

    1. Abe H.,
    2. Yamaguchi-Shinozaki K.,
    3. Urao T.,
    4. Iwasaki T.,
    5. Hosokawa D.,
    6. Shinozaki K.
    (1997) Role of Arabidopsis Myc and Myb homologs in drought-and abscisic acid-regulated gene expression. Plant Cell 9, 1859–1868
    OpenUrlAbstract/FREE Full Text
    1. Alvarez J.,
    2. Smyth D. R.
    (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126, 2377–2386
    OpenUrlAbstract
    1. Atchley W. R.,
    2. Fitch W. M.
    (1997) A natural classification of the basic Helix-Loop-Helix class of transcription factors. Proc. Natl. Acad. Sci. USA 94, 5172–5176
    OpenUrlAbstract/FREE Full Text
    1. Bernard O.,
    2. Cory S.,
    3. Gerondakis S.,
    4. Webb E.,
    5. Adams J.M.
    (1983) Sequence of the murine and human cellular myc oncogenes and two modes of myc transcription resulting from chromosome translocation in B lymphoid tumours. EMBOJ 2, 2375–2383
    OpenUrlPubMedWeb of Science
    1. Bowman J. L.,
    2. Smyth D. R.
    (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126, 2387–2396
    OpenUrlAbstract
    1. Bowman J. L.,
    2. Smyth D. R.,
    3. Meyerowitz E. M.
    (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112, 1–20
    OpenUrlAbstract
    1. Braissant O.,
    2. Wahli W.
    (1998) A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1, 10–16
    OpenUrl
    1. Cai M.,
    2. Davis R. W.
    (1990) Yeast centromere binding protein Cbf1 of the Helix-Loop-Helix protein family is required for chromosome stability and methionine prototrophy. Cell 61, 437–446
    OpenUrlCrossRefPubMedWeb of Science
    1. Daingwall C.,
    2. Laskey R. A.
    (1991) Nuclear targeting sequence a consensus?. Trends Biochem. Sci 16, 478–481
    OpenUrlCrossRefPubMedWeb of Science
    1. Damiani R. D.,
    2. Wessler S. R.
    (1993) An upstream open reading frame represses expression of Lc, a member of the R/B family of maize transcriptional activators. Proc. Natl. Acad. Sci. USA 90, 8244–8248
    OpenUrlAbstract/FREE Full Text
    1. Drews G.,
    2. Bowman J.,
    3. Meyerowitz E.
    (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65, 991–1002
    OpenUrlCrossRefPubMedWeb of Science
    1. Elliott R. C.,
    2. Betzner A. S.,
    3. Huttner E.,
    4. Oakes M. P.,
    5. Tucker W. Q. J.,
    6. Gerentes D.,
    7. Perez P.,
    8. Smyth D. R.
    (1996) AINTEGUMENTA, an APETALA2 -like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8, 155–168
    OpenUrlAbstract/FREE Full Text
    1. Endrizzi K.,
    2. Moussian B.,
    3. Haecker A.,
    4. Levin J. Z.,
    5. Laux T.
    (1996) The shoot meristemless gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10, 967–979
    OpenUrlCrossRefPubMedWeb of Science
    1. Ferrandiz C.,
    2. Liljegren S. J.,
    3. Yanofsky M. F.
    (2000) FRUITFULL negatively regulates the SHATTERPROOF genes during Arabidopsis development. Science 289, 436–438
    OpenUrlAbstract/FREE Full Text
    1. Fisher D. E.,
    2. Parent L. A.,
    3. Sharp P. A.
    (1993) High affinity DNA-binding Myc analogs: Recognition by an alpha helix. Cell 72, 467–476
    OpenUrlCrossRefPubMedWeb of Science
    1. Flanagan C. A.,
    2. Hu Y.,
    3. Ma H.
    (1996) Specific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. Plant J 10, 343–353
    OpenUrlCrossRefPubMedWeb of Science
    1. Goff S. A.,
    2. Cone K. C.,
    3. Chandler V. L.
    (1992) Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev 6, 864–875
    OpenUrlAbstract/FREE Full Text
    1. Goodrich J.,
    2. Carpenter R.,
    3. Coen E. S.
    (1992) A common gene regulates pigmentation pattern in diverse plant species. Cell 68, 955–964
    OpenUrlCrossRefPubMedWeb of Science
    1. Grill E.,
    2. Somerville C.
    (1991) Construction and characterization of a yeast artificial chromosome library of Arabidopsis which is suitable for chromosome walking. Mol. Gen. Genet 226, 484–490
    OpenUrlPubMedWeb of Science
    1. Gu Q.,
    2. Ferrandiz C.,
    3. Yanofsky M. F.,
    4. Martienssen R.
    (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 1509–1517
    OpenUrlAbstract
    1. Guilfoyle T.,
    2. Hagen G.,
    3. Ulmasov T.,
    4. Murfett J.
    (1998) How does auxin turn on genes?. Plant Physiol 118, 341–347
    OpenUrlFREE Full Text
    1. Jofuku K. D.,
    2. den Boer B. G. W.,
    3. Van Montagu M.,
    4. Okamuro J. K.
    (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6, 1211–1225
    OpenUrlAbstract/FREE Full Text
    1. Liljegren S. J.,
    2. Ditta G. S.,
    3. Eshed Y.,
    4. Savidge B.,
    5. Bowman J. L.,
    6. Yanofsky M. F.
    (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766–770
    OpenUrlCrossRefPubMedWeb of Science
    1. Liu Z.,
    2. Franks R. G.,
    3. Klink V. P.
    (2000) Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA. Plant Cell 12, 1879–1891
    OpenUrlAbstract/FREE Full Text
    1. Long J. A.,
    2. Moan E. I.,
    3. Medford J. I.,
    4. Barton M. K.
    (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69
    OpenUrlCrossRefPubMedWeb of Science
    1. Mandel M. A.,
    2. Yanofsky M. F.
    (1995) The Arabidopsis AGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell 7, 1763–1771
    OpenUrlAbstract/FREE Full Text
    1. Nemhauser J.,
    2. Feldman L. J.,
    3. Zambryski P. C.
    (2000) Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127, 3877–3888
    OpenUrlAbstract
    1. Ni M.,
    2. Tepperman J. M.,
    3. Quail P. H.
    (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic Helix-Loop-Helix protein. Cell 95, 657–667
    OpenUrlCrossRefPubMedWeb of Science
    1. Perrot G. H.,
    2. Cone K. C.
    (1989) Nucleotide sequence of the maize R-S gene. Nucl. Acids Res 17, 8003–.
    OpenUrlFREE Full Text
    1. Quattrocchio F.,
    2. Wing J. F.,
    3. Van der Woude K.,
    4. Mol J. N. M.,
    5. Koes R.
    (1998) Analysis of bHLH and MYB domain proteins: species specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J 13, 475–488
    OpenUrlCrossRefPubMedWeb of Science
    1. Radicella J. P.,
    2. Turks D.,
    3. Chandler V. L.
    (1991) Cloning and nucleotide sequence of a cDNA encoding B-Peru, a regulatory protein of the anthocyanin pathway in maize. Plant Mol. Biol 17, 127–130
    OpenUrlCrossRefPubMedWeb of Science
    1. Rost B.,
    2. Sander C.
    (1994) Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19, 55–72
    OpenUrlCrossRefPubMedWeb of Science
    1. Savidge B.,
    2. Rounsley S. D.,
    3. Yanofsky M. F.
    (1995) Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7, 721–733
    OpenUrlAbstract/FREE Full Text
    1. Sessions R. A.
    (1997) Arabidopsis (Brassicaceae) flower development and gynoecium patterning in wild type and ETTIN mutants. Am. J. Bot 84, 1179–1191
    OpenUrlAbstract/FREE Full Text
    1. Sessions A.,
    2. Nemhauser J.,
    3. McCall A.,
    4. Roe J. L.,
    5. Feldmann K. A.,
    6. Zambryski P. C.
    (1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124, 4481–4491
    OpenUrlAbstract
    1. Sessions R. A.,
    2. Zambryski P. C.
    (1995) Arabidopsis gynoecium structure in the wild type and in ettin mutants. Development 121, 1519–1532
    OpenUrlAbstract
    1. Sieber M.,
    2. Allemann R. K.
    (1998) Arginine (348) is a major determinant of the DNA binding specificity of transcription factor E12. Biol. Chem 379, 731–735
    OpenUrl
    1. Smyth D. R.,
    2. Bowman J. L.,
    3. Meyerowitz E. M.
    (1990) Early flower development in Arabidopsis. Plant Cell 2, 755–767
    OpenUrlAbstract/FREE Full Text
    1. Terryn N.,
    2. et al
    . (1999) Evidence for an ancient chromosomal duplication in Arabidopsis thaliana by sequencing and analyzing a 400-kb contig at the APETALA2 locus on chromosome 4. FEBS Lett 445, 237–245
    OpenUrlCrossRefPubMedWeb of Science
    1. Ulmasov T.,
    2. Hagen G.,
    3. Guilfoyle T. J.
    (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276, 1865–1868
    OpenUrlAbstract/FREE Full Text
    1. Ulmasov T.,
    2. Hagen G.,
    3. Guilfoyle T. J.
    (1999) Dimerization and DNA binding of auxin response factors. Plant J 19, 309–319
    OpenUrlCrossRefPubMedWeb of Science
    1. Voronova A.,
    2. Baltimore D.
    (1990) Mutations that disrupt DNA binding and dimer formation in the E47 helix-loop-helix protein map to distinct domains. Proc. Natl. Acad. Sci. USA 87, 4722–4726
    OpenUrlAbstract/FREE Full Text
    1. Ward E. R.,
    2. Jen G. C.
    (1990) Isolation of single-copy-sequence clones from a yeast artificial chromosome library of randomly-sheared Arabidopsis thaliana DNA. Plant Mol. Biol 14, 561–568
    OpenUrlCrossRefPubMedWeb of Science
    1. Weigel D.,
    2. Alvarez J.,
    3. Smyth D. R.,
    4. Yanofsky M. F.,
    5. Meyerowitz E. M.
    (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843–859
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein
M.G. Heisler, A. Atkinson, Y.H. Bylstra, R. Walsh, D.R. Smyth
Development 2001 128: 1089-1098;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights