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Research Article

Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato

Ali Ahmad Naz, Smita Raman, Ciera C. Martinez, Neelima R. Sinha, Gregor Schmitz, and Klaus Theres
  1. aMax Planck Institute for Plant Breeding Research, 50829 Cologne, Germany; and
  2. bDepartment of Plant Biology, University of California, Davis, CA 95616

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PNAS February 5, 2013 110 (6) 2401-2406; https://doi.org/10.1073/pnas.1214300110
Ali Ahmad Naz
aMax Planck Institute for Plant Breeding Research, 50829 Cologne, Germany; and
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Smita Raman
aMax Planck Institute for Plant Breeding Research, 50829 Cologne, Germany; and
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Ciera C. Martinez
bDepartment of Plant Biology, University of California, Davis, CA 95616
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Neelima R. Sinha
bDepartment of Plant Biology, University of California, Davis, CA 95616
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Gregor Schmitz
aMax Planck Institute for Plant Breeding Research, 50829 Cologne, Germany; and
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Klaus Theres
aMax Planck Institute for Plant Breeding Research, 50829 Cologne, Germany; and
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  • For correspondence: theres@mpipz.mpg.de
  1. Edited* by Maarten Koornneef, Max Planck Institute for Plant Breeding Research, Cologne, Germany, and approved December 21, 2012 (received for review August 17, 2012)

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Abstract

Leaf morphology and the pattern of shoot branching determine to a large extent the growth habit of seed plants. Until recently, the developmental processes that led to the establishment of these morphological structures seemed unrelated. Here, we show that the tomato Trifoliate (Tf) gene plays a crucial role in both processes, affecting the formation of leaflets in the compound tomato leaf and the initiation of axillary meristems in the leaf axil. Tf encodes a myeloblastosis oncoprotein (MYB)-like transcription factor related to the Arabidopsis thaliana LATERAL ORGAN FUSION1 (LOF1) and LOF2 proteins. Tf is expressed in the leaf margin, where leaflets are formed, and in the leaf axil, where axillary meristems initiate. During tomato ontogeny, expression of Tf in young leaf primordia increases, correlating with a rise in leaf dissection (heteroblasty). Formation of leaflets and initiation of axillary meristems can be traced back to groups of pluripotent cells. Tf function is required to inhibit differentiation of these cells and thereby to maintain their morphogenetic competence, a fundamental process in plant development. KNOTTED1-LIKE proteins, which are known regulators in tomato leaf dissection, require Tf activity to exert their function in the basal part of the leaf. Similarly, the plant hormone auxin needs Tf activity to initiate the formation of lateral leaflets. Thus, leaf dissection and shoot branching rely on a conserved mechanism that regulates the morphogenetic competence of cells at the leaf margin and in the leaf axil.

Footnotes

  • ↵1Present address: Institute of Crop Science and Resource Conservation, Rheinische Friedrich-Wilhelms-Universität Bonn, D-53115 Bonn, Germany.

  • ↵2Present address: Institute for Evolution and Biodiversity, D-48149 Münster, Germany

  • ↵3To whom correspondence should be addressed. E-mail: theres{at}mpipz.mpg.de.
  • Author contributions: A.A.N., N.R.S., G.S., and K.T. designed research; A.A.N., S.R., C.C.M., and G.S. performed research; A.A.N., S.R., C.C.M., N.R.S., G.S., and K.T. analyzed data; and A.A.N., S.R., C.C.M., N.R.S., G.S., and K.T. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. JX522478).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1214300110/-/DCSupplemental.

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Tf modulates leaf and shoot architecture
Ali Ahmad Naz, Smita Raman, Ciera C. Martinez, Neelima R. Sinha, Gregor Schmitz, Klaus Theres
Proceedings of the National Academy of Sciences Feb 2013, 110 (6) 2401-2406; DOI: 10.1073/pnas.1214300110

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Tf modulates leaf and shoot architecture
Ali Ahmad Naz, Smita Raman, Ciera C. Martinez, Neelima R. Sinha, Gregor Schmitz, Klaus Theres
Proceedings of the National Academy of Sciences Feb 2013, 110 (6) 2401-2406; DOI: 10.1073/pnas.1214300110
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Proceedings of the National Academy of Sciences: 110 (6)
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