microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development

Authors

  • Geraldo Felipe Ferreira e Silva,

    1. Laboratory of Molecular Genetics of Plant Development, Department of Genetics, Instituto de Biociências, State University of Sao Paulo, Botucatu, Sao Paulo, Brazil
    2. Centro de Biotecnologia Agricola, Escola Superior de Agricultura ‘Luiz de Queiroz’, University of Sao Paulo, Piracicaba, Sao Paulo, Brazil
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  • Eder Marques Silva,

    1. Laboratory of Molecular Genetics of Plant Development, Department of Genetics, Instituto de Biociências, State University of Sao Paulo, Botucatu, Sao Paulo, Brazil
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  • Mariana da Silva Azevedo,

    1. Laboratory of Hormonal Control of Plant Development, Department of Biological Sciences, Escola Superior de Agricultura ‘Luiz de Queiroz’, University of Sao Paulo, Piracicaba, Sao Paulo, Brazil
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  • Mike Anderson Corazon Guivin,

    1. Laboratory of Molecular Genetics of Plant Development, Department of Genetics, Instituto de Biociências, State University of Sao Paulo, Botucatu, Sao Paulo, Brazil
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  • Daniel Alves Ramiro,

    1. Centro de Biotecnologia Agricola, Escola Superior de Agricultura ‘Luiz de Queiroz’, University of Sao Paulo, Piracicaba, Sao Paulo, Brazil
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  • Cassia Regina Figueiredo,

    1. Laboratory of Hormonal Control of Plant Development, Department of Biological Sciences, Escola Superior de Agricultura ‘Luiz de Queiroz’, University of Sao Paulo, Piracicaba, Sao Paulo, Brazil
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  • Helaine Carrer,

    1. Centro de Biotecnologia Agricola, Escola Superior de Agricultura ‘Luiz de Queiroz’, University of Sao Paulo, Piracicaba, Sao Paulo, Brazil
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  • Lázaro Eustáquio Pereira Peres,

    1. Laboratory of Hormonal Control of Plant Development, Department of Biological Sciences, Escola Superior de Agricultura ‘Luiz de Queiroz’, University of Sao Paulo, Piracicaba, Sao Paulo, Brazil
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  • Fabio Tebaldi Silveira Nogueira

    Corresponding author
    1. Laboratory of Molecular Genetics of Plant Development, Department of Genetics, Instituto de Biociências, State University of Sao Paulo, Botucatu, Sao Paulo, Brazil
    2. Centro de Biotecnologia Agricola, Escola Superior de Agricultura ‘Luiz de Queiroz’, University of Sao Paulo, Piracicaba, Sao Paulo, Brazil
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Summary

Fruit ripening in tomato (Solanum lycopersicum L.) is well understood at the molecular level. However, information regarding genetic pathways associated with tomato ovary and early fruit development is still lacking. Here, we investigate the possible role(s) of the microRNA156/SQUAMOSA promoter-binding protein-like (SPL or SBP box) module (miR156 node) in tomato ovary development. miR156-targeted S. lycopersicum SBP genes were dynamically expressed in developing flowers and ovaries, and miR156 was mainly expressed in meristematic tissues of the ovary, including placenta and ovules. Transgenic tomato cv. Micro-Tom plants over-expressing the AtMIR156b precursor exhibited abnormal flower and fruit morphology, with fruits characterized by growth of extra carpels and ectopic structures. Scanning electron microscopy and histological analyses showed the presence of meristem-like structures inside the ovaries, which are probably responsible for the ectopic organs. Interestingly, expression of genes associated with meristem maintenance and formation of new organs, such as LeT6/TKN2 (a KNOX-like class I gene) and GOBLET (a NAM/CUC-like gene), was induced in developing ovaries of transgenic plants as well as in the ovaries of the natural mutant Mouse ear (Me), which also displays fruits with extra carpels. Conversely, expression of the MADS box genes MACROCALYX (MC) and FUL1/TDR4, and the LEAFY ortholog FALSIFLORA, was repressed in the developing ovaries of miR156 over-expressors, suggesting similarities with Arabidopsis at this point of the miR156/SPL pathway but with distinct functional consequences in reproductive development. Altogether, these observations suggest that the miR156 node is involved in maintenance of the meristematic state of ovary tissues, thereby controlling initial steps of fleshy fruit development and determinacy.

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