Article,

S(1) basic leucine zipper transcription factors shape plant architecture by controlling C/N partitioning to apical and lateral organs

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Proc Natl Acad Sci U S A, 121 (7): e2313343121 (2024)Kreisz, Philipp Hellens, Alicia M Froschel, Christian Krischke, Markus Maag, Daniel Feil, Regina Wildenhain, Theresa Draken, Jan Braune, Gabriel Erdelitsch, Leon Cecchino, Laura Wagner, Tobias C Ache, Peter Mueller, Martin J Becker, Dirk Lunn, John E Hanson, Johannes Beveridge, Christine A Fichtner, Franziska Barbier, Francois F Weiste, Christoph eng 408153945/Deutsche Forschungsgemeinschaft (DFG)/ CE200100015/Department of Education and Training | ARC | Australian Research Council Centre of Excellence for Plant Success in Nature and Agriculture (ARC CoE for Plant Success in Nature and Agriculture)/ 2024/02/05 Proc Natl Acad Sci U S A. 2024 Feb 13;121(7):e2313343121. doi: 10.1073/pnas.2313343121. Epub 2024 Feb 5..
DOI: 10.1073/pnas.2313343121

Abstract

Plants tightly control growth of their lateral organs, which led to the concept of apical dominance. However, outgrowth of the dormant lateral primordia is sensitive to the plant's nutritional status, resulting in an immense plasticity in plant architecture. While the impact of hormonal regulation on apical dominance is well characterized, the prime importance of sugar signaling to unleash lateral organ formation has just recently emerged. Here, we aimed to identify transcriptional regulators, which control the trade-off between growth of apical versus lateral organs. Making use of locally inducible gain-of-function as well as single and higher-order loss-of-function approaches of the sugar-responsive S(1)-basic-leucine-zipper (S(1)-bZIP) transcription factors, we disclosed their largely redundant function in establishing apical growth dominance. Consistently, comprehensive phenotypical and analytical studies of S(1)-bZIP mutants show a clear shift of sugar and organic nitrogen (N) allocation from apical to lateral organs, coinciding with strong lateral organ outgrowth. Tissue-specific transcriptomics reveal specific clade III SWEET sugar transporters, crucial for long-distance sugar transport to apical sinks and the glutaminase GLUTAMINE AMIDO-TRANSFERASE 1_2.1, involved in N homeostasis, as direct S(1)-bZIP targets, linking the architectural and metabolic mutant phenotypes to downstream gene regulation. Based on these results, we propose that S(1)-bZIPs control carbohydrate (C) partitioning from source leaves to apical organs and tune systemic N supply to restrict lateral organ formation by C/N depletion. Knowledge of the underlying mechanisms controlling plant C/N partitioning is of pivotal importance for breeding strategies to generate plants with desired architectural and nutritional characteristics.

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