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WIREs Dev Biol

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Pathfinding in angiosperm reproduction: pollen tube guidance by pistils ensures successful double fertilization

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Ravishankar Palanivelu, Tatsuya Tsukamoto

Published Online: Nov 18 2011

DOI: 10.1002/wdev.6

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Abstract Sexual reproduction in flowering plants is unique in multiple ways. Distinct multicellular gametophytes contain either a pair of immotile, haploid male gametes (sperm cells) or a pair of female gametes (haploid egg cell and homodiploid central cell). After pollination, the pollen tube, a cellular extension of the male gametophyte, transports both male gametes at its growing tip and delivers them to the female gametes to affect double fertilization. The pollen tube travels a long path and sustains its growth over a considerable amount of time in the female reproductive organ (pistil) before it reaches the ovule, which houses the female gametophyte. The pistil facilitates the pollen tube's journey by providing multiple, stage‐specific, nutritional, and guidance cues along its path. The pollen tube interacts with seven different pistil cell types prior to completing its journey. Consequently, the pollen tube has a dynamic gene expression program allowing it to continuously reset and be receptive to multiple pistil signals as it migrates through the pistil. Here, we review the studies, including several significant recent advances, that led to a better understanding of the multitude of cues generated by the pistil tissues to assist the pollen tube in delivering the sperm cells to the female gametophyte. We also highlight the outstanding questions, draw attention to opportunities created by recent advances and point to approaches that could be undertaken to unravel the molecular mechanisms underlying pollen tube–pistil interactions. WIREs Dev Biol 2012, 1:96–113. doi: 10.1002/wdev.6 This article is categorized under: Plant Development > Gametophyte Development Plant Development > Fertilization, Embryogenesis, and Seed Development Plant Development > Inflorescence, Flower, and Fruit Development Additional Supporting Information may be found in the online version of this article. Movie1‐Palanivelu‐Tsukamoto.mov Movie1‐Palanivelu‐Tsukamoto.mov

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Diagram of early events during pollen tube growth in an Arabidopsis pistil. (1) Desiccated pollen grain (oval shaped) adhering to a stigmatic papillar cell. (2) Pollen coat ‘foot formation’ (pink area between the pollen grain and the stigmatic papillar cell) after completion of hydration (pollen grain is now round shaped). (3) Pollen tube (red) germination, and (4) pollen tube growth toward the style.

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Pollen tube growth and guidance to ovule micropyle. (a) Diagram of pollen tube growth within an Arabidopsis pistil. Pollen grains (p) on the stigma (si) germinate and extend pollen tubes (PT, red) through the style (st) and transmitting tract (TT) before entering one of the two ovary (ov) chambers to target an ovule (o). (b) Diagram of a female gametophyte within an ovule. m, micropyle; ac, antipodal cells. The central cell has a homodipoid nucleus, and therefore, its nucleus is larger than the haploid nuclei in the synergid, egg, and antipodal cells. (c) Diagram showing a pollen tube (PT) approaching the ovule containing a mature female gametophyte. Prior to pollen tube arrival in the ovule micropyle, all three antipodal cells degenerate (dac). spc, two sperm cells inside a pollen tube; vn, vegetative nucleus (nucleus of the pollen tube cell); sc, synergid cell; ec, egg cell; cc, central cell.

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Putative FER signaling pathway in an Arabidopsis synergid cell prior to or at the arrival of the pollen tube. (1) Binding of an unknown ligand from either the female gametophyte (FG, 1a) or the pollen tube (PT, 1b) with FER results in (2) autophosphorylation of FER receptor‐like kinase, initiating (3) an uncharacterized signaling pathway which perhaps redistributes NTA to pollen tube entry site in the synergid cell, leading to (4) generation of a secreted signal that ultimately (5) culminates in inducing pollen tube reception/growth arrest. Question marks indicate putative steps.

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Major events during pollen tube–female gametophyte interactions in plant reproduction. The genes (based on mutant analysis) that mediate indicated steps in the pollen tube–female gametophyte interactions. Question marks indicate that the placement of the gene in that position is based on data that tested only in some of the steps shown in this figure. Genes marked with an asterisk are known to function in pollen tubes. PT, pollen tube.

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Temporal sequence of pollen tube–female gametophyte interactions within an ovule during Arabidopsis reproduction (left to right). The hallmark event at each step is indicated and only the micropylar region of an ovule is shown at each step. Egg cell is shaded in yellow, two synergid cells and central cell are shaded in green and grey, respectively.

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Diagram of pollen tube growth on the septum and ovule of an Arabidopsis pistil. Several pollen tubes (red) emerge from the transmitting tract and traverse the septum. However, typically only one pollen tube approaches the funiculus and then targets the ovule micropyle. FG, female gametophyte.

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Resources

Movie 1. Description of the Arabidopsis semi-in vivo pollen tube guidance assay. This time-lapse movie describes the steps that need to be undertaken to set up the assay as previously described.³⁴ The assay can be used to monitor pollen tube-ovule interactions. Since the assay is modular, any combination of the three components of the assay (pollen, stigma/style and ovules) can be tested, including genetically impossible combinations such as the behavior of wild type pollen tubes grown through a wild-type pistil with mutant ovules.

Movie 2. Ovule targeting by a pollen tube in the Arabidopsis semi-in vivo pollen tube guidance assay. After emerging from the style, a pollen tube grows on the pollen growth medium, approaches an ovule, enters through the micropyle, reaches the female gametophyte, arrests growth and explosively discharges its cytoplasmic contents. In this example, pollen tube is marked with LAT52:GFP and was germinated through a wild-type pistil and allowed to approach a wild-type ovule. Time elapsed is shown in minutes (min). Scale bar is shown in the lower right.

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