J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (1): 121-142.DOI: 10.1111/jipb.13606

• Metabolism and Biochemistry • Previous Articles     Next Articles

Antagonistic MADS-box transcription factors SEEDSTICK and SEPALLATA3 form a transcriptional regulatory network that regulates seed oil accumulation

Shuangcheng He1†, Yuanchang Min1†, Zijin Liu1†, Fang Zhi2, Rong Ma1, Ankang Ge1, Shixiang Wang1, Yu Zhao1, Danshuai Peng1, Da Zhang1, Minshan Jin1, Bo Song1, Jianjun Wang1, Yuan Guo1 and Mingxun Chen1*   

  1. 1. State Key Laboratory for Crop Stress Resistance and High‐Efficiency Production, National Yangling Agricultural Biotechnology & Breeding Center, Shaanxi Key Laboratory of Crop Heterosis, College of Agronomy, Northwest A&F University, Yangling 712100, China;
    2. State Key Laboratory for Crop Stress Resistance and High‐Efficiency Production, Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Yangling 712100, China
    These authors contributed equally to this work.
    *Correspondence: Mingxun Chen (cmx786@nwafu.edu.cn)
  • Received:2023-09-13 Accepted:2023-12-26 Online:2023-12-26 Published:2024-01-01

Abstract: Transcriptional regulation is essential for balancing multiple metabolic pathways that influence oil accumulation in seeds. Thus far, the transcriptional regulatory mechanisms that govern seed oil accumulation remain largely unknown. Here, we identified the transcriptional regulatory network composed of MADS-box transcription factors SEEDSTICK (STK) and SEPALLATA3 (SEP3), which bridges several key genes to regulate oil accumulation in seeds. We found that STK, highly expressed in the developing embryo, positively regulates seed oil accumulation in Arabidopsis (Arabidopsis thaliana). Furthermore, we discovered that SEP3 physically interacts with STK in vivo and in vitro. Seed oil content is increased by the SEP3 mutation, while it is decreased by SEP3 overexpression. The chromatin immunoprecipitation, electrophoretic mobility shift assay, and transient dual-luciferase reporter assays showed that STK positively regulates seed oil accumulation by directly repressing the expression of MYB5, SEP3, and SEED FATTY ACID REDUCER 4 (SFAR4). Moreover, genetic and molecular analyses demonstrated that STK and SEP3 antagonistically regulate seed oil production and that SEP3 weakens the binding ability of STK to MYB5, SEP3, and SFAR4. Additionally, we demonstrated that TRANSPARENT TESTA 8 (TT8) and ACYL-ACYL CARRIER PROTEIN DESATURASE 3 (AAD3) are direct targets of MYB5 during seed oil accumulation in Arabidopsis. Together, our findings provide the transcriptional regulatory network antagonistically orchestrated by STK and SEP3, which fine tunes oil accumulation in seeds.

Key words: seed oil accumulation, SEP3, STK, transcription factor, transcriptional regulation

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