State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.
University of Chinese Academy of Sciences, Beijing 100049, China.
Plant Cell. 2024 Sep 3;36(9):3824-3837. doi: 10.1093/plcell/koae206.
Germline fate determination is a critical event in sexual reproduction. Unlike animals, plants specify the germline by reprogramming somatic cells at the late stages of their development. However, the genetic basis of germline fate determination and how it evolved during the land plant evolution are still poorly understood. Here, we report that the plant homeodomain finger protein GERMLINE IDENTITY DETERMINANT (GLID) is a key regulator of the germline specification in liverwort, Marchantia polymorpha. Loss of the MpGLID function causes failure of germline initiation, leading to the absence of sperm and egg cells. Remarkably, the overexpression of MpGLID in M. polymorpha induces the ectopic formation of cells with male germline cell features exclusively in male thalli. We further show that MpBONOBO (BNB), with an evolutionarily conserved function, can induce the formation of male germ cell-like cells through the activation of MpGLID by directly binding to its promoter. The Arabidopsis (Arabidopsis thaliana) MpGLID ortholog, MALE STERILITY1 (AtMS1), fails to replace the germline specification function of MpGLID in M. polymorpha, demonstrating that a derived function of MpGLID orthologs has been restricted to tapetum development in flowering plants. Collectively, our findings suggest the presence of the BNB-GLID module in complex ancestral land plants that has been retained in bryophytes, but rewired in flowering plants for male germline fate determination.
生殖细胞命运决定是有性生殖中的一个关键事件。与动物不同，植物通过在其发育后期重新编程体细胞来指定生殖细胞。然而，生殖细胞命运决定的遗传基础以及它在陆地植物进化过程中是如何进化的，仍然知之甚少。在这里，我们报道了植物同源结构域手指蛋白 GERMLINE IDENTITY DETERMINANT（GLID）是苔藓植物 Marchantia polymorpha 生殖细胞特化的关键调节因子。MpGLID 功能丧失会导致生殖细胞起始失败，导致精子和卵子缺失。值得注意的是，MpGLID 在 M. polymorpha 中的过表达仅在雄性叶状体中诱导具有雄性生殖细胞特征的细胞的异位形成。我们进一步表明，具有进化上保守功能的 MpBONOBO（BNB）可以通过直接结合其启动子激活 MpGLID，从而诱导具有雄性生殖细胞样细胞的形成。拟南芥（Arabidopsis thaliana）的 MpGLID 同源物 MALE STERILITY1（AtMS1）未能替代 M. polymorpha 中 MpGLID 的生殖细胞特化功能，表明 MpGLID 同源物的衍生功能已局限于开花植物的绒毡层发育。总的来说，我们的研究结果表明，复杂的祖代陆地植物中存在 BNB-GLID 模块，该模块在苔藓植物中保留下来，但在开花植物中重新布线，用于雄性生殖细胞命运决定。
