The bHLH proteins BEE and BIM positively modulate the shade avoidance syndrome in Arabidopsis seedlings

Authors

  • Nicolás Cifuentes-Esquivel,

    1. Centre for Research in Agricultural Genomics (CRAG), Consejo Superior de Investigaciones Científicas (CSIC) – Institut de Recerca i Tecnologia Agroalimentàries (IRTA) – Universitat Autòmona de Barcelona (UAB) – Universitat de Barcelona (UB), Barcelona 08193, Spain
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  • Jordi Bou-Torrent,

    Corresponding author
    1. Centre for Research in Agricultural Genomics (CRAG), Consejo Superior de Investigaciones Científicas (CSIC) – Institut de Recerca i Tecnologia Agroalimentàries (IRTA) – Universitat Autòmona de Barcelona (UAB) – Universitat de Barcelona (UB), Barcelona 08193, Spain
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  • Anahit Galstyan,

    1. Centre for Research in Agricultural Genomics (CRAG), Consejo Superior de Investigaciones Científicas (CSIC) – Institut de Recerca i Tecnologia Agroalimentàries (IRTA) – Universitat Autòmona de Barcelona (UAB) – Universitat de Barcelona (UB), Barcelona 08193, Spain
    Current affiliation:
    1. Department of Biology, University of Washington, Seattle, WA 98195, USA
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  • Marçal Gallemí,

    1. Centre for Research in Agricultural Genomics (CRAG), Consejo Superior de Investigaciones Científicas (CSIC) – Institut de Recerca i Tecnologia Agroalimentàries (IRTA) – Universitat Autòmona de Barcelona (UAB) – Universitat de Barcelona (UB), Barcelona 08193, Spain
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  • Giovanna Sessa,

    1. Institute of Molecular Biology and Pathology, National Research Council, Rome 00185, Italy
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  • Mercè Salla Martret,

    1. Centre for Research in Agricultural Genomics (CRAG), Consejo Superior de Investigaciones Científicas (CSIC) – Institut de Recerca i Tecnologia Agroalimentàries (IRTA) – Universitat Autòmona de Barcelona (UAB) – Universitat de Barcelona (UB), Barcelona 08193, Spain
    Current affiliation:
    1. Department of Pathology and Experimental Therapeutic, University of Barcelona, Hospitalet de Llobregat 08907, Spain
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  • Irma Roig-Villanova,

    1. Centre for Research in Agricultural Genomics (CRAG), Consejo Superior de Investigaciones Científicas (CSIC) – Institut de Recerca i Tecnologia Agroalimentàries (IRTA) – Universitat Autòmona de Barcelona (UAB) – Universitat de Barcelona (UB), Barcelona 08193, Spain
    Current affiliation:
    1. Dipartamento de Bioscienze, Università degli Studi di Milano, Milano 20133, Italy
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  • Ida Ruberti,

    1. Institute of Molecular Biology and Pathology, National Research Council, Rome 00185, Italy
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  • Jaime F. Martínez-García

    Corresponding author
    1. Centre for Research in Agricultural Genomics (CRAG), Consejo Superior de Investigaciones Científicas (CSIC) – Institut de Recerca i Tecnologia Agroalimentàries (IRTA) – Universitat Autòmona de Barcelona (UAB) – Universitat de Barcelona (UB), Barcelona 08193, Spain
    2. Institució Catalana de Recerca i Estudis Avançats, Barcelona 08010, Spain
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Summary

The shade avoidance syndrome (SAS) refers to a set of plant responses initiated after perception by the phytochromes of light with a reduced red to far-red ratio, indicative of vegetation proximity or shade. These responses, including elongation growth, anticipate eventual shading from potential competitor vegetation by overgrowing neighboring plants or flowering to ensure production of viable seeds for the next generation. In Arabidopsis thaliana seedlings, the SAS includes dramatic changes in gene expression, such as induction of PHYTOCHROME RAPIDLY REGULATED 1 (PAR1), encoding an atypical basic helix-loop-helix (bHLH) protein that acts as a transcriptional co-factor to repress hypocotyl elongation. Indeed, PAR1 has been proposed to act fundamentally as a dominant negative antagonist of conventional bHLH transcription factors by forming heterodimers with them to prevent their binding to DNA or other transcription factors. Here we report the identification of PAR1-interacting factors, including the brassinosteroid signaling components BR-ENHANCED EXPRESSION (BEE) and BES1-INTERACTING MYC-LIKE (BIM), and characterize their role as networked positive regulators of SAS hypocotyl responses. We provide genetic evidence that these bHLH transcriptional regulators not only control plant growth and development under shade and non-shade conditions, but are also redundant in the control of plant viability. Our results suggest that SAS responses are initiated as a consequence of a new balance of transcriptional regulators within the pre-existing bHLH network triggered by plant proximity, eventually causing hypocotyls to elongate.

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