Wang Xin, Liu Jiaxin, Shang Erlei, Hawar Amangul, Ito Toshiro, Sun Bo
State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing 210023, China.
Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan.
Plant Cell. 2024 Oct 7;36(12):5004-22. doi: 10.1093/plcell/koae273.
Brassinosteroid (BR) signaling and the C-class MADS-box gene AGAMOUS (AG) play important roles in ovule development in Arabidopsis (Arabidopsis thaliana). However, how BR signaling integrates with AG functions to control the female reproductive process remains elusive. Here, we showed that the regulatory role of BR signaling in proper ovule development is mediated by the transcriptional repressor gene ZINC FINGER PROTEIN 11 (ZFP11), which is a direct target of AG. ZFP11 expression initiates from the placenta upon AG induction and becomes prominent in the funiculus of ovule primordia. Plants harboring zfp11 mutations showed reduced placental length with decreased ovule numbers and some aborted ovules. During ovule development, the transcription factor BRASSINAZOLE-RESISTANT 1 (BZR1), which functions downstream of BR signaling, inhibits ZFP11 expression in the chalaza and nucellus. Weakened BR signaling leads to stunted integuments in ovules, resulting from the direct repression of INNER NO OUTER (INO) and WUSCHEL (WUS) by extended ZFP11 expression in the chalaza and nucellus, respectively. In addition, the zfp11 mutant shows reduced sensitivity to BR biosynthesis inhibitors and can rescue outer integument defects in brassinosteroid insensitive 1 (bri1) mutants. Thus, the precise spatial regulation of ZFP11, which is activated by AG in the placenta and suppressed by BR signaling in the central and distal regions of ovules, is essential for ensuring sufficient ovule numbers and proper ovule formation.
油菜素类固醇(BR)信号传导和C类MADS盒基因AGAMOUS(AG)在拟南芥(Arabidopsis thaliana)胚珠发育中起重要作用。然而,BR信号如何与AG功能整合以控制雌性生殖过程仍不清楚。在这里,我们表明BR信号在正常胚珠发育中的调节作用是由转录抑制基因锌指蛋白11(ZFP11)介导的,ZFP11是AG的直接靶标。ZFP11的表达在AG诱导下从胎座开始,并在胚珠原基的珠柄中变得明显。携带zfp11突变的植物胎座长度缩短,胚珠数量减少,一些胚珠败育。在胚珠发育过程中,BR信号下游起作用的转录因子油菜素唑抗性1(BZR1)抑制合点和珠心处的ZFP11表达。BR信号减弱导致胚珠中珠被发育不良,这分别是由于合点和珠心中ZFP11表达延长直接抑制了内外珠被(INO)和WUSCHEL(WUS)所致。此外,zfp11突变体对BR生物合成抑制剂的敏感性降低,并且可以挽救油菜素类固醇不敏感1(bri1)突变体的外珠被缺陷。因此,ZFP11的精确空间调控对于确保足够的胚珠数量和正常的胚珠形成至关重要,ZFP11在胎座中被AG激活,在胚珠的中部和远端区域被BR信号抑制。