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Shoot Branching and Leaf Dissection in Tomato Are Regulated by Homologous Gene Modules

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Busch, Bernhard L., Schmitz, Gregor, Rossmann, Susanne, Piron, Florence, Ding, Jia, Bendahmane, Abdelhafid, Theres, Klaus·2011·The Plant Cell
DOI 10.1105/tpc.111.087981PMC PMC3229137
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Abstract

Aerial plant architecture is predominantly determined by shoot branching and leaf morphology, which are governed by apparently unrelated developmental processes, axillary meristem formation, and leaf dissection. Here, we show that in tomato (Solanum lycopersicum), these processes share essential functions in boundary establishment. Potato leaf (C), a key regulator of leaf dissection, was identified to be the closest paralog of the shoot branching regulator Blind (Bl). Comparative genomics revealed that these two R2R3 MYB genes are orthologs of the Arabidopsis thaliana branching regulator REGULATOR OF AXILLARY MERISTEMS1 (RAX1). Expression studies and complementation analyses indicate that these genes have undergone sub- or neofunctionalization due to promoter differentiation. C acts in a pathway independent of other identified leaf dissection regulators. Furthermore, the known leaf complexity regulator Goblet (Gob) is crucial for axillary meristem initiation and acts in parallel to C and Bl. Finally, RNA in situ hybridization revealed that the branching regulator Lateral suppressor (Ls) is also expressed in leaves. All four boundary genes, C, Bl, Gob, and Ls, may act by suppressing growth, as indicated by gain-of-function plants. Thus, leaf architecture and shoot architecture rely on a conserved mechanism of boundary formation preceding the initiation of leaflets and axillary meristems.

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  • Loss-of-function mutants of LAS show fusion of lateral branches to the main axis.

    “| LAS | Ls (tomato), MOC1 (rice | GRAS | Fusion of lateral branches to | SAM and lateral organs, | Schumacher et al. (1999); Li et al. |”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Busch et al. (2011)

    The Results (page unavailable) say that Ls mutations manifest only as a lack of axillary meristems. The same section attributes side-shoot fusions to bl mutants, not Ls mutants. Although the Discussion broadly mentions organ fusions among boundary-gene mutants, it does not identify fusion of lateral branches to the main axis as an Ls phenotype. (LLM, conf=0.86)

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  • In addition to LAS, RAX1, BL, and C influence axillary meristem development.

    “In addition to LAS, the MYB factors REGULATOR OF AXILLARY MERISTEMS1 (RAX1) in Arabidopsis (Keller et al., 2006), as well as BLIND (BL) and POTATO LEAF (C) in tomato (Schmitz et al., 2002; Busch et al., 2011), influence axillary meristem development.”

    From Shaping plant architecture (2015) · cites this paper as Busch et al., 2011

    The Introduction states that tomato BLIND and Arabidopsis RAX genes regulate axillary meristem formation, and the Results report impaired axillary bud initiation in bl mutants. The paper identifies C as a related tomato gene expressed in boundary zones, but its reported mutant phenotype concerns leaf development; the Results say c plants otherwise develop normally. It therefore does not establish the attributed effect of C on axillary meristem development. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • These MYB genes are specifically expressed in the leaf axil and plants homozygous for loss-of-function alleles show fusions of axillary shoots to their subtending leaves or to the main axis, indicating the gene product is required for axillary meristem formation and organ separation.

    “These genes are specifically expressed in the leaf axil and plants homozygous for loss-of-function alleles show fusions of axillary shoots to their subtending leaves or to the main axis (Greb et al., 2003;Busch et al., 2011), indicating that the respective gene product is required not only for axillary meristem formation, but also for organ separation.”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Busch et al., 2011

    Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

  • Potato leaf is expressed in the boundaries between initiating leaflets and represses growth in these regions.

    “Potato leaf is expressed in the boundaries between initiating leaflets and represses growth in these regions (Busch et al., 2011).”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Busch et al., 2011

    The Results section reports that Potato leaf (C) is expressed at the proximal and distal boundaries of young leaflet primordia. The Discussion proposes that C may repress growth in boundary regions, based partly on growth retardation when C is misexpressed. The claim presents this proposed function as established. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Loss-of-function mutants of LAS have a reduced number of tillers and spikelets.

    “| | | | number of tillers and | | |”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Busch et al. (2011)

    The Results (page unavailable) state that mutations in tomato Ls cause a lack of axillary meristems, supporting a branching defect. The paper does not report that LAS loss-of-function mutants have fewer tillers or spikelets; searches for those terms found no such finding. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

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Authors
Busch, B. L., Schmitz, G., Rossmann, S., Piron, F., Ding, J., Bendahmane, A., & Theres, K.
Affiliations
  • Max Planck Institute for Plant Breeding Research (DE)
  • Unité de Recherche en Génomique Végétale, Unité Mixte de Recherche, Institut National de la Recherche Agronomique–Centre National de la Recherche Scientifique, 91057 Evry cedex, France
  • Centre National de la Recherche Scientifique (FR)
ORCID
Venue
The Plant Cell
Publisher
Oxford University Press (OUP)
Published
2011-10-01
Volume
23
Issue
10
Pages
3595-3609
ISSN
  • 1040-4651 (ISSN-L)
  • 1532-298X
DOI
10.1105/tpc.111.087981
PMC
PMC3229137
OpenAlex
W1998228679
Cited by
122
References
7
Citations by year
2026: 5 · 2025: 8 · 2024: 7 · 2023: 15 · 2022: 9 · 2021: 7 · 2020: 8 · 2019: 6 · 2018: 7 · 2017: 7 · 2016: 16 · 2015: 7 · 2014: 6 · 2013: 8 · 2012: 4
FWCI
7.33
Type
journal article
Language
en
Open access
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations
  • The Plant Cell (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
Institute of Materials Research and Engineering
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
tomato, shoot branching, leaf dissection, leaf architecture, axillary meristem initiation, boundary formation, neofunctionalization, orthologs, comparative genomics
MeSH terms
Genetic Complementation Test, Mutation, Phenotype, Plant Proteins, Promoter Regions, Genetic, Sequence Alignment, Arabidopsis, In Situ Hybridization, Sequence Analysis, DNA, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Plant Leaves, Plant Shoots, Solanum lycopersicum, DNA, Plant, Genome, Plant, RNA, Plant, Plants, Genetically Modified, Gene Regulatory Networks

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