Signaling at Physical Barriers during Pollen-Pistil Interactions

Abstract

In angiosperms, double fertilization requires pollen tubes to transport non-motile sperm to distant egg cells housed in a specialized female structure known as the pistil, mediating the ultimate fusion between male and female gametes. During this journey, the pollen tube encounters numerous physical barriers that must be mechanically circumvented, including the penetration of the stigmatic papillae, style, transmitting tract, and synergid cells as well as the ultimate fusion of sperm cells to the egg or central cell. Additionally, the pollen tube must maintain structural integrity in these compact environments, while responding to positional guidance cues that lead the pollen tube to its destination. Here, we discuss the nature of these physical barriers as well as efforts to genetically and cellularly identify the factors that allow pollen tubes to successfully, specifically, and quickly circumnavigate them.

Keywords: cell adhesion; cell–cell interaction; pectin; plant cell wall; pollen penetration.

Figure 1

Schematics of physical barriers encountered by the pollen tube. An Arabidopsis pistil is shown with various physical barriers that are encountered by the pollen tube. (A) Pollen grain foot formation, hydration and subsequent pollen tube germination occurs at the stigmatic papillae, and pollen tube growth occurs between the cell wall and plasma membrane layers. (B) Possible barriers encountered by the pollen tube are displayed including penetration of (1) the stigmatic papillae, (2) the stigma-style interface, and (3) the transmitting tract. The fourth pollen tube has successfully penetrated through these barriers and is descending through the transmitting tract. (C) Germinating pollen tubes navigating the transmitting tract receive guidance cues that prompt pollen tubes to exit the transmitting tract tissues and begin moving along a funiculus to reach the ovule. (D) The ovule is penetrated by the pollen tube via the micropylar opening. The pollen tube then penetrates the degenerating synergid cell. Subsequent bursting and delivery of the sperm cell nuclei are imminent.

Figure 2

Schematic of physical barriers encountered by a germinating pollen tube at the style and transmitting tract. (A) Enlarged view of a germinating pollen tube navigating the tightly-packed style tissue. (B) The ANX1/2-BUPS1/2-LLG2/3 signaling complex is localized to the tip of the growing pollen tube and binds pollen tube-secreted RALF4/19, functioning as an autocrine signaling loop to prevent premature bursting. RopGEFs interact with the ANX1/2-BUPS1/2-LLG2/3 complex while activating ROP1, resulting in exocytic trafficking that may be essential for mechanotransduction signaling to occur for the pollen tube to exit the stigma-style interface (C) As the pollen tube penetrates further down the loosely packed transmitting tract, the pistil-produed γ-Amino-Butyric Acid (GABA) concentration gradient grows higher and Transmitting Tissue Specific (TTS) Arabinogalactan Proteins (AGPs) increase in abundance, both signaling to the pollen tube that it is navigating in the correct direction.

Figure 3

Schematic of a pollen tube being attracted to an ovule and synergid penetration. (A) The pollen tube exits the transmitting tract and moves along the funiculus. (B) While approaching the ovule, PRK6, a receptor-like kinase, binds LURE peptides secreted by the synergid cells, acting as a positive reinforcement signal. AMOR glycans, potentially attached to AGPs, potentiate this attractive signal. (C) The pollen tube enters the ovule by penetrating a synergid cell. (D) As the pollen tube penetrates the filiform apparatus, and subsequently the synergid, it is prompted to burst. The pollen tube’s ANX1/2-BUPS1/2-LLG2/3 signaling complex binds RALF34, secreted by the filiform apparatus, and the ovule’s FER-HERK1/ANJ-LRE signaling complex potentially binds unidentified RALFs, secreted by the pollen tube. FER-HERK1/ANJ-LRE signaling results in Reactive Oxygen Species (ROS) accumulation in the filiform apparatus, facilitating pollen tube bursting. (E) Sperm cell fuses with the egg and central cells to form the new embryo and endosperm tissue, respectively. Pectins surrounding the ovule become de-methylesterified. Nitric oxide (NO) species are released into the surrounding area. NO species nitrosate and inactivate LURE peptides, working synergistically with the rigidifying pectin to prevent polytubey.