Stop and go signals at the stigma–pollen interface of the Brassicaceae

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The key evolutionary innovation of the angiosperm closed carpel has resulted in the physical separation of the male gametophyte, which is housed in the pollen grain, and the female gametophyte, which is embedded in the ovule deep inside the ovary at the base of the pistil. Consequently, fertilization in angiosperms requires that the pollen tube and its cargo of haploid sperm cells travel through many layers of somatic pistil tissue. This journey starts at the receptive stigma surface to which pollen grains adhere and where they hydrate and germinate, continues with extracellular growth of the pollen tube through the stigma, style, and ovary, and culminates in entry of the pollen tube into the ovule, release of its sperm cells, and double fertilization. Throughout this journey, an intricate molecular dialogue between cells of the pistil and the pollen grain or pollen tube determines if pollination will ultimately result in fertilization and seed production or in interruption of pollen tube growth, failure of fertilization, and lack of fruit and seed (Johnson et al. 2019). In this way, pistil tissues function as selective gatekeepers that save female tissue resources and safeguard their ovules from unproductive fusions by discriminating against inappropriate (incompatible) pollen grains or tubes, be they derived from the same species (conspecific) or from different species (heterospecific), while allowing appropriate (compatible) pollen grains or tubes to effect fertilization. The site in the pistil where discrimination against incompatible pollen occurs is dictated by the structural and biochemical characteristics of the stigma and the way in which pollen grains, which are released from anthers in a highly desiccated and metabolically inactive state, access water for hydration and subsequent metabolic activation. The surface properties of the stigma differ among plant families. In some families, the stigma is covered by an abundant exudate from which pollen grains can readily access water. As a result, these stigmas allow indiscriminate hydration and germination of conspecific and heterospecific pollen grains alike, and arrest of inappropriate pollen tubes must therefore occur within internal tissues of the pistil, most often in the style. By contrast, families such as the Brassicaceae, in which the stigma lacks abundant exudate, hydration of pollen grains can only occur upon release of water from the stigma. Thus, in these families, the pollen–stigma interaction is a highly regulated and selective process in which the stigma plays a critical role in determining the fate of pollen grains, with pollen hydration representing a major reproductive checkpoint. Here, I present an overview of the complex molecular processes that underlie the cell-cell recognition events that take place at the pollen–stigma interface with a focus on the Brassicaceae (crucifers), a family in which these events have been extensively analyzed. After a description of the stigma–pollen interface, the review will highlight major results relating to (i) compatible pollinations for completion of the plant's life cycle, (ii) discrimination between self- and nonself-pollen for enforcing outbreeding and avoiding the deleterious effects of inbreeding, and (iii) discrimination between conspecific and heterospecific pollen for conservation of pistil resources and maintenance of species integrity. 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