Pollen and Stigma Structure and Function: The Role of Diversity in Pollination

Abstract

Pollination in Arabidopsis. (A) Diagram of one of the two ovary chambers after removal of the ovary wall (OW). Pollen lands on the stigma, where it hydrates, germinates, and extends a tube that enters the transmitting tract (TT). The tube emerges onto the septum (S), grows up the funiculus (f), and enters the micropyle opening of the ovule (O), where it fertilizes the egg and central cell. The position of the transmitting tract inside the septum is shown in the cross-section at the bottom of the pistil. (B) Transmission electron micrograph showing the point of contact between a pollen grain (P) and a stigma papillus (S), colorized to highlight the pollen coat (pink), intine (peach), exine (green), stigma cell wall (yellow), and stigma cuticle (blue). A foot of lipid-rich material (arrows) collects between the two surfaces. The thin stigma pellicle that covers the cuticle is not distinct here. (C) Diagram of early events on the stigma, including adhesion (1), pollen coat “foot” formation and pollen hydration (2), pollen tube emergence from the grain (3), and pollen tube invasion of the papillae cell wall and extension toward the style (4). (D) to (F) Sequence of early events during Arabidopsis pollination. (D) The pollen coat has mobilized to the site of contact between the pollen and the stigma, forming a foot between the two surfaces (arrow), as visualized with the lipid dye FM1-43. (E) The pollen tube (arrow) has emerged from the grain's exine wall and projects itself into the stigma papillus, as visualized with the cell wall dye Congo red. (F) Pollen tubes (arrow) wind their way toward the style, moving between the cell walls of the papillae, where they are protected from the Congo red dye. Angiosperm reproduction is highly selective. Female tissues are able to discriminate between pollen grains, recognizing pollen from the appropriate species while rejecting pollen from unrelated species (or from the same plant in self-incompatible species). This selectivity is accompanied by tremendous diversity in the cell surfaces of male and female reproductive structures. The uniquely rich fossil record of pollen wall structures has been of great benefit. Literally hundreds of years of scientific effort have focused on integrating the diversity of pollen form with angiosperm taxonomy. Linking these morphological differences to functional roles is more challenging, requiring molecular and genetic assays that reveal purpose not only within a species but across diverse taxa. Here, we first survey advances in the cellular and molecular understanding of angiosperm pollen and stigma biology, including pollen–stigma adhesion, pollen hydration and germination, and pollen tube emergence and invasion. By capitalizing on microscopy, molecular, genetic, and genomic resources, it is possible to magnify and dissect cellular functions at the pollen and stigma surfaces both before and after they make contact (Table 1 Pollen and Stigma Structural Features and Their Roles Pollen and Stigma Structural Features and Their Roles Mature angiosperm pollen grains are unusual vegetative cells that contain within themselves sperm cells, complete with cell walls and plasma membranes. This arrangement is accomplished soon after meiosis, when an asymmetric mitotic division produces a large cell that engulfs its diminutive sister, the generative cell (Twell et al., 1998; Yang and Sundaresan, 2000). Subsequently, the generative cell undergoes a second mitosis to form the second sperm cell required for double fertilization; “tricellular” pollen completes this division before it is released from the anther, whereas “bicellular” pollen undergoes this division only later, within the elongating pollen tube. These categories do not apply to gymnosperm pollen grains, which can contain a score of cells and differ from angiosperm pollen in several other respects (Pacini et al., 1999). Pollen cells are contained within a unique pollen wall, whose construction begins when the meiocyte is newly formed, with the surface layers elaborated over time. At maturity, the pollen surface can be divided into three principal strata, with the relative amount of each varying between species: (1) an outer exine wall, itself multilayered, composed of the chemically resistant polymer sporopollenin and interrupted by openings called apertures; (2) an inner intine, also sometimes multilayered, made primarily of cellulose; and (3) a pollen coat, composed of lipids, proteins, pigments, and aromatic compounds, that fills the sculptured cavities of the pollen exine (Figure 1B). Stigmas, the receptive portions of the female tissues, bind pollen and mediate tube migration into the style. Stigmas generally are classified into two groups: wet stigmas, which are covered with surface cells that often lyse to release a viscous surface secretion containing proteins, lipids, polysaccharides, and pigments; and dry stigmas, which have intact surface cells that typically protrude as papillae