Three Stylists Pattern the Fine Architectures of Apical Gynoecium and are Critical for Male Gametophyte-Pistil Interaction

The gynoecium, a central floral organ and the main autapomorphy of the angiosperms, is derived from the fusion of carpels originating evolutionarily from modified leaves, and considered as having evolved from a simple setup followed by adaptive adjustment in cell type and tissue distribution to facilitate efficient sexual reproduction. As a sequence of the adjustment, the apical tissues of the gynoecium differentiated into the stigma where pollen germinates and the style where pollen tubes grow. Both the structural patterning and functional specification of stigma and the style are critical for plant fertility. However, the molecular mechanisms that regulate the structural and functional specification of these essential tissues of the female reproductive organ remain largely unknown, especially, how the fine structures of stigma and style are established at the interface receiving and interreacting with pollen and pollen tubes remain to be elucidated. Here, we report a novel angiosperm-specific gene family, STIGMA & STYLE STYLIST 1-3 (SSS1, SSS2, SSS3). The SSS1 expressed predominately in the transmitting tract tissue of style, SSS2 intensively in stigma and SSS3 mainly in stylar peripheral region round the transmitting tract. SSSs coregulate the patterning of the apical gynoecium via control of cell expansion or elongation. Both the architecture and function of apical gynoecium were affected by the alteration of SSS genes expression levels, indicating their critical roles in the establishment of a proper female interface for communication with pollen or pollen tubes. Further investigations revealed that the NGATHA3 (NGA3) transcription factor can directly bind to SSSs promoter and control SSSs expression. Over-expression of SSSs could rescue the stylar defect of nga1nga3 double mutant, indicating their context in the same regulatory pathway. Our findings reveal a novel molecular mechanism responsible for the patterning of the fine architecture of stigma and style and establishing a proper interface for pollen germination and pollen tube growth, and therefore crucial for plant sexual reproduction. We also reveal novel function of NGA as an activator, but not as a repressor.

Keywords: gynoecium, stigma, style, NGATHA

Suggested Citation: Suggested Citation

Li, Wenwei and Huang, Xiaorong and Zou, Jie and Wu, Jianjun and Jiao, Hengwu and Peng, Xiongbo and Sun, Meng-Xiang, Three Stylists Pattern the Fine Architectures of Apical Gynoecium and are Critical for Male Gametophyte-Pistil Interaction. Available at SSRN: https://ssrn.com/abstract=3578155 or http://dx.doi.org/10.2139/ssrn.3578155

This version of the paper has not been formally peer reviewed.