Invasion of the stigma by the pollen tube or an oomycete pathogen: striking similarities and differences

Abstract

The epidermis is the first barrier that protects organisms from surrounding stresses. Similar to the hyphae of filamentous pathogens that penetrate and invade the outer tissues of the host, the pollen germinates and grows a tube within epidermal cells of the stigma. Early responses of the epidermal layer are therefore decisive for the outcome of these two-cell interaction processes. Here, we aim at characterizing and comparing how the papillae of the stigma respond to intrusion attempts, either by hypha of the hemibiotrophic oomycete root pathogen, Phytophthora parasitica or by the pollen tube. We found that P. parasitica spores attach to the papillae and hyphae subsequently invade the entire pistil. Using transmission electron microscopy, we examined in detail the invasive growth characteristics of P. parasitica and found that the hypha passed through the stigmatic cell wall to grow in contact with the plasma membrane, contrary to the pollen tube that advanced engulfed within the two cell wall layers of the papilla. Further quantitative image analysis revealed that the pathogen and the pollen tube trigger reorganization of the endomembrane system (trans Golgi network, late endosome) and the actin cytoskeleton. Some of these remodeling processes are common to both invaders, while others appear to be more specific showing that the stigmatic cells trigger an appropriate response to the invading structure and somehow can recognize the invader that attempts to penetrate.