Cited by 39Plant Molecular Biology ResearchPlant Parasitism and ResistanceDevelopmental Biology and Gene Regulation

Lateral suppressor and Goblet act in hierarchical order to regulate ectopic meristem formation at the base of tomato leaflets

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Rossmann, Susanne, Kohlen, Wouter, Hasson, Alice, Theres, Klaus·2015·The Plant Journal

Abstract

Summary: In seed plants, new axes of growth are established by the formation of meristems, groups of pluripotent cells that maintain themselves and initiate the formation of lateral organs. After embryonic development, secondary shoot meristems form in the boundary zones between the shoot apical meristem and leaf primordia, the leaf axils. In addition, many plant species develop ectopic meristems at different positions of the plant body. In the compound tomato leaf, ectopic meristems can initiate at the base of leaflets, which are delimited by two distinct boundary zones, referred to as the proximal ( PLB ) and distal ( DLB ) leaflet boundaries. We demonstrate that the two leaflet boundaries differ from each other and that ectopic meristem formation is strictly limited to the DLB . Our data suggest that the DLB harbours a group of pluripotent cells that seems to be the launching pad for meristem formation. Initiation of these meristems is dependent on the activities of the transcriptional regulators Goblet ( Gob ) and Lateral suppressor ( Ls ), specifically expressed in the DLB . Gob and Ls act in hierarchical order, because Ls transcript accumulation is dependent on Gob activity, but not vice versa. Ectopic meristem formation at the DLB is also observed in other seed plants, like Cardamine pratensis , indicating that it is part of a widespread developmental program. Ectopic meristem formation leads to an increase in the number of buds, enhances the capacity for survival and opens the route to vegetative propagation.

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  • Cells at distal leaflet boundaries of tomato and Cardamine pratensis are less differentiated, lack differentiation markers such as stomata or trichomes, and exhibit down-regulation of Histone H4 mRNA accumulation, indicating a low cell division rate.

    “At the same time, these cells are less differentiated, as indicated by the lack of differentiation markers, such as stomata or trichomes, and exhibit a down-regulation of Histone H4 mRNA accumulation, indicating a low cell division rate (Rossmann et al., 2015; Fig. 1d).”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Rossmann et al., 2015

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

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  • NAM/CUC3 gene expression in the distal leaflet boundary is evolutionarily conserved in many compound leaved species, such as Aquilegia caerulea, S. tuberosum, C. hirsuta, P. sativum and C. pratensis.

    “NAM/ CUC3 gene expression in the distal leaflet boundary is evolutionarily conserved in many compound leaved species, such as Aquilegia caerulea, S. tuberosum, C. hirsuta, P. sativum and C. pratensis (Blein et al., 2008;Berger et al., 2009;Rossmann et al., 2015).”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Rossmann et al., 2015

    The “Ectopic meristem formation beyond tomato” section (page not specified in our copy) reports CpCUC2 and CpCUC3 expression in distal leaflet boundaries of C. pratensis, and the paper discusses the homologous Gob gene in tomato. It does not establish the claimed expression pattern across all the listed species; C. hirsuta appears in the methods as the source of probes, not as a species in which expression was demonstrated. (LLM, conf=0.87)

    Experimental — accuracy not yet measured
  • Distal leaflet boundaries of tomato and Cardamine pratensis leaves harbor smaller cells compared with surrounding tissues.

    “The distal leaflet boundaries of tomato and Cardamine pratensis leaves were shown to harbor smaller cells in comparison to surrounding tissues (Rossmann et al., 2015).”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Rossmann et al., 2015

  • The two genes Ls and Gob act in hierarchical order, with Ls being downstream of Gob, to initiate new meristems at distal leaflet boundaries.

    “Genetic experiments and expression studies suggest that the two genes act in hierarchical order, with Ls being downstream of Gob, to initiate new meristems at distal leaflet boundaries (Rossmann et al., 2015).”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Rossmann et al., 2015

  • The leaf axil and the distal leaflet boundary harbor pluripotent cell groups that retain the competence for meristem formation.

    “The patterns of cell division and the absence of well-known differentiation markers, such as stomata and trichomes, indicate that the leaf axil and the distal leaflet boundary harbor pluripotent cell groups that retain the competence for meristem formation (Rossmann et al., 2015).”

    From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Rossmann et al., 2015

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Cites

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Research works printed but not linked: 8

  1. Bell, E.M., Lin, W.-C., Husbands, A.Y., Yu, L., Jaganatha, V., Jablonska, B., Mangeon, A., Neff, M.M., Girke, T. and Springer, P.S. (2012) Arabidopsis LATERAL ORGAN BOUNDARIES negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc. Natl Acad. Sci. USA, 109, 21146-21151.
  2. Efroni, I., Eshed, Y. and Lifschitz, E. (2010) Morphogenesis of simple and compound leaves: a critical review. Plant Cell, 22, 1019-1032.
  3. Klime sov a, J. and Klime s, L. (2007) Bud banks and their role in vegetative regeneration-a literature review and proposal for simple classification and assessment. Perspect. Plant Ecol. Evol. Syst. 8, 115-129.
  4. Komatsu, K., Maekawa, M., Ujiie, S., Satake, Y., Furutani, I., Okamoto, H., Shimamoto, K. and Kyozuka, J. (2003) LAX and SPA: major regulators of shoot branching in rice. Proc. Natl Acad. Sci. USA, 100, 11765-11770.
  5. Salisbury, E. (1965) The reproduction of Cardamine pratensis L. and Card- amine palustris Peterman particularly in relation to their specialized foliar vivipary, and its deflexion of the constraints of natural selection. Proc. R. Soc. Lond. B Biol. Sci. 163, 321-342.
  6. Schmitz, G., Tillmann, E., Carriero, F., Fiore, C., Cellini, F. and Theres, K. (2002) The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc. Natl Acad. Sci. USA, 99, 1064-1069.
  7. Schumacher, K., Schmitt, T., Rossberg, M., Schmitz, G. and Theres, K. (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc. Natl Acad. Sci. USA, 96, 290-295.
  8. Steeves, T.A. and Sussex, I.M. (1989) Patterns in Plant Development. Cam- bridge: Cambridge University Press.

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Authors
Rossmann, S., Kohlen, W., Hasson, A., & Theres, K.
Affiliations
Max Planck Institute for Plant Breeding Research (DE)
Corresponding author
Theres, Klaus
Venue
The Plant Journal
Publisher
Wiley
Published
2015-03
Volume
81
Issue
6
Pages
837-848
ISSN
  • 0960-7412 (ISSN-L)
  • 1365-313X
OpenAlex
W2098266028
Cited by
39
References
11
Citations by year
2026: 2 · 2025: 2 · 2024: 3 · 2023: 5 · 2022: 1 · 2021: 4 · 2020: 6 · 2019: 4 · 2017: 4 · 2016: 4 · 2015: 4
FWCI
4.84
Type
journal article
Language
en
Open access
Locations
  • The Plant Journal (publishedVersion)
  • PubMed (publishedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
  • Deutsche Forschungsgemeinschaft (FE552/12-1)
  • Alexander von Humboldt-Stiftung (1146256)
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
goblet, compound leaf development, tomato, transcriptional regulation, pluripotent cells, vegetative propagation, Cardamine pratensis, shoot apical meristem
MeSH terms
Mutation, Phenotype, Plant Proteins, Transcription Factors, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Plant Leaves, Meristem, Plant Shoots, Solanum lycopersicum, Plants, Genetically Modified

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