Three STIGMA AND STYLE STYLISTs Pattern the Fine Architectures of Apical Gynoecium and Are Critical for Male Gametophyte-Pistil Interaction

Abstract

The gynoecium is derived from the fusion of carpels and is considered to have evolved from a simple setup followed by adaptive adjustment in cell type and tissue distribution to facilitate efficient sexual reproduction [1, 2]. As a sequence of the adjustment, the apical gynoecium differentiates into a stigma and a style. Both the structural patterning and functional specification of the apical gynoecium are critical for plant fertility [3, 4]. However, how the fine structures of the apical gynoecium are established at the interface interacting with pollen and pollen tubes remain to be elucidated. Here, we report a novel angiosperm-specific gene family, STIGMA AND STYLE STYLIST 1-3 (SSS1, SSS2, and SSS3). The SSS1 expresses predominately in the transmitting tract tissue of style, SSS2 expresses intensively in stigma, and SSS3 expresses mainly in stylar peripheral region round the transmitting tract. SSSs coregulate the patterning of the apical gynoecium via controlling cell expansion or elongation. Both the architecture and function of apical gynoecium can be affected by the alteration of SSS expression, indicating their critical roles in the establishment of a proper female interface for communication with pollen tubes. The NGATHA3 (NGA3) transcription factor [5, 6] can directly bind to SSSs promoter and control SSSs expression. Overexpression 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 patterning the fine architecture of apical gynoecium and establishing a proper interface for pollen tube growth, which is therefore crucial for plant sexual reproduction.