An incoherent feed‐forward loop involving bHLH transcription factors, Auxin and CYCLIN‐Ds regulates style radial symmetry establishment in Arabidopsis

• Published in: The Plant journal : for cell and molecular biology 2024-09, Vol.119 (6), p.2885-2903
• Main Authors: Tasker‐Brown, William, Koh, Samuel W. H., Trozzi, Nicola, Maio, Kestrel A., Jamil, Iqra, Jiang, Yuxiang, Majda, Mateusz, Smith, Richard S., Moubayidin, Laila
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; auxin; Auxins; Basic Helix-Loop-Helix Transcription Factors - genetics; Basic Helix-Loop-Helix Transcription Factors - metabolism; Biological activity; Cell cycle; Cell Division; Cellular manufacture; cell‐division orientation; Cyclin D - genetics; Cyclin D - metabolism; CYCLIN‐D1; 1; CYCLIN‐D3; 3; Defects; Fertilization; Flowers - genetics; Flowers - growth & development; Flowers - metabolism; G1 phase; G1‐phase progression; Gene Expression Regulation, Plant; Gene regulation; Genetic analysis; gynoecium; Helix-loop-helix proteins (basic); incoherent feed‐forward loop; Indoleacetic Acids - metabolism; Morphogenesis; Mutation; Pattern formation; Plant layout; radial symmetry; Reproductive organs; style development; Symmetry; Transcription factors; transcriptional regulation
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16959

SUMMARY The bilateral‐to‐radial symmetry transition occurring during the development of the Arabidopsis thaliana female reproductive organ (gynoecium) is a crucial biological process linked to plant fertilization and seed production. Despite its significance, the cellular mechanisms governing the establishment and breaking of radial symmetry at the gynoecium apex (style) remain unknown. To fill this gap, we employed quantitative confocal imaging coupled with MorphoGraphX analysis, in vivo and in vitro transcriptional experiments, and genetic analysis encompassing mutants in two bHLH transcription factors necessary and sufficient to promote transition to radial symmetry, SPATULA (SPT) and INDEHISCENT (IND). Here, we show that defects in style morphogenesis correlate with defects in cell‐division orientation and rate. We showed that the SPT‐mediated accumulation of auxin in the medial‐apical cells undergoing symmetry transition is required to maintain cell‐division‐oriented perpendicular to the direction of organ growth (anticlinal, transversal cell division). In addition, SPT and IND promote the expression of specific core cell‐cycle regulators, CYCLIN‐D1;1 (CYC‐D1;1) and CYC‐D3;3, to support progression through the G1 phase of the cell cycle. This transcriptional regulation is repressed by auxin, thus forming an incoherent feed‐forward loop mechanism. We propose that this mechanism fine‐tunes cell division rate and orientation with the morphogenic signal provided by auxin, during patterning of radial symmetry at the style. Significance Statement Our work reveals the cellular basis underpinning a bilateral‐to‐radial symmetry transition occurring during the development of the Arabidopsis female reproductive organ. To promote the medial‐apical fusion of the developing carpels, two bHLH transcription factors, SPATULA and INDEHISCENT, orchestrate auxin accumulation in specific cells to maintain anticlinal cell‐division orientation and fine‐tune progression through the G1 cell‐cycle phase via an Incoherent type‐I Feed‐Forward Loop (I‐IFFL).