A Ploidy-Sensitive Mechanism Regulates Aperture Formation on the Arabidopsis Pollen Surface and Guides Localization of the Aperture Factor INP1

摘要

Pollen presents a powerful model for studying mechanisms of precise formation and deposition of extracellular structures. Deposition of the pollen wall exine leads to the generation of species-specific patterns on pollen surface. In most species, exine does not develop uniformly across the pollen surface, resulting in the formation of apertures–openings in the exine that are species-specific in number, morphology and location. A long time ago, it was proposed that number and positions of apertures might be determined by the geometry of tetrads of microspores–the precursors of pollen grains arising via meiotic cytokinesis, and by the number of last-contact points between sister microspores. We have tested this model by characterizing Arabidopsis mutants with ectopic apertures and/or abnormal geometry of meiotic products. Here we demonstrate that contact points per se do not act as aperture number determinants and that a correct geometric conformation of a tetrad is neither necessary nor sufficient to generate a correct number of apertures. A mechanism sensitive to pollen ploidy, however, is very important for aperture number and positions and for guiding the aperture factor INP1 to future aperture sites. In the mutants with ectopic apertures, the number and positions of INP1 localization sites change depending on ploidy or ploidy-related cell size and not on INP1 levels, suggesting that sites for aperture formation are specified before INP1 is brought to them. Author Summary Deposition of extracellular materials next to a cell can protect the cell, change its morphology, or help it to move and communicate. To be able to perform such functions, extracellular materials must be deposited very precisely, but how cells achieve such precision is mostly unknown. A beautiful example of a very precisely deposited extracellular structure is the wall surrounding pollen grains. Pollen from different species often looks remarkably different–in part, because wall materials are deposited at some places on pollen surface and absent from others. The places where the wall is absent are called apertures and they are species-specific in shape, number, and positions. This suggests that developing pollen consistently marks some of its surface regions as different from the rest of the surface to allow them to develop into apertures. Aperture number and positions were long thought to be determined by geometric arrangement of pollen precursors arising during meiotic division and by the number of last-contact points between these cells. Here we challenge this model by using Arabidopsis mutants with abnormal arrangement of meiotic products or the number of last-contact points and by demonstrating that these factors are neither necessary nor sufficient for aperture placement. In contrast, we find that a mechanism sensitive to pollen ploidy–with cells responding to factors dependent either on ploidy itself or on cell size–is very important for aperture number and positions.