Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato
Open accessAbstract
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.
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Loss-of-function mutants of LOF1-2 show organ fusions.
“| LOF1-2 | T f(tomato) | MYB | Organ fusions, reduced | Stem and cauline leaves, | Lee et al. (2009); Naz et al. (2013) |”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Naz et al. (2013)
The Arabidopsis LOF1 and LOF2 genes encode MYB protein family proteins.
“| LOF1-2 | T f(tomato) | MYB | Organ fusions, reduced | Stem and cauline leaves, | Lee et al. (2009); Naz et al. (2013) |”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Naz et al. (2013)
LOF1-2 is expressed in the boundary between the stem and cauline leaves, inflorescence meristem and young floral primordia, and floral organs.
“| LOF1-2 | T f(tomato) | MYB | Organ fusions, reduced | Stem and cauline leaves, | Lee et al. (2009); Naz et al. (2013) |”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Naz et al. (2013)
Tf in tomato is homologous to Arabidopsis LOF1-2.
“| LOF1-2 | T f(tomato) | MYB | Organ fusions, reduced | Stem and cauline leaves, | Lee et al. (2009); Naz et al. (2013) |”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Naz et al. (2013)
Loss-of-function mutants of LOF1-2 have simpler leaves in compound-leaf species.
“| | | | leaves in compound-leaf | and young floral | |”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Naz et al. (2013)
Loss-of-function mutants of LOF1-2 have a reduced number of axillary meristems.
“| | | | number of AMs, simpler | inflorescence meristem | |”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Naz et al. (2013)
Cites
The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves
Berger, Y., Harpaz-Saad, S., Brand, A., Melnik, H., Sirding, N., Alvarez, J. P., Zinder, M., Samach, A., Eshed, Y., & Ori, N. (2009) · Development · doi:10.1242/dev.031625 · Cited by 305 · see citing works
Organogenetic capacity of leaves: The significance of marginal blastozones in angiosperms
Hagemann, W., & Gleissberg, S. (1996) · Plant Systematics and Evolution · doi:10.1007/bf00984901 · Cited by 205 · see citing works
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<i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems
Wang, Q., Hasson, A., Rossmann, S., & Theres, K. (2016) · New Phytologist · doi:10.1111/nph.13641 · Cited by 106 · see citing works
Self-citation
- Authors
- Naz, A. A., Raman, S., Martinez, C. C., Sinha, N. R., Schmitz, G., & Theres, K.
- Affiliations
- Max Planck Society (DE)
- University of California, Davis (US)
- Max Planck Institute for Plant Breeding Research (DE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-01-22
- Volume
- 110
- Issue
- 6
- Pages
- 2401-2406
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3568312
- OpenAlex
- W2016601088
- Cited by
- 73
- References
- 2
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 6 · 2023: 7 · 2022: 6 · 2021: 4 · 2020: 6 · 2019: 6 · 2018: 2 · 2017: 5 · 2016: 4 · 2015: 10 · 2014: 5 · 2013: 3
- FWCI
- 8.86
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- National Science Foundation (FOOD-CT-2006-016214)
- Weizmann Institute of Science
- Hebrew University of Jerusalem
- Max-Planck-Gesellschaft
- National Institutes of Health (5r25gm078441-18)
- National Institute of General Medical Sciences (R25-GM078441)
- Division of Graduate Education
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- MYB transcription factors, compound leaf, axillary meristem initiation, shoot branching, pluripotent cells, auxin, leaf margin, leaf ontogeny
- MeSH terms
- Amino Acid Sequence, Base Sequence, Indoleacetic Acids, Microscopy, Electron, Scanning, Molecular Sequence Data, Mutation, Phylogeny, Plant Growth Regulators, Plant Proteins, Transcription Factors, Genes, Plant, Sequence Homology, Amino Acid, Homeodomain Proteins, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Plant Leaves, Meristem, Plant Shoots, Solanum lycopersicum, DNA, Plant, Plants, Genetically Modified
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