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Chemical Signaling for Pollen Tube Guidance at a Glance Yoko Mizuta1,2,* and Tetsuya Higashiyama1,3

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Chemical Signaling for Pollen Tube Guidance at a Glance Yoko Mizuta1,2,* and Tetsuya Higashiyama1,3 © 2018. Published by The Company of Biologists Ltd | Journal of Cell Science (2018) 131, jcs208447. doi:10.1242/jcs.208447 CELL SCIENCE AT A GLANCE SPECIAL ISSUE: PLANT CELL BIOLOGY Chemical signaling for pollen tube guidance at a glance Yoko Mizuta1,2,* and Tetsuya Higashiyama1,3 ABSTRACT further discuss the precise one-to-one guidance system that exists Pollen tube guidance is a unique navigating system that is required for in multi-ovular plants. The pollen tube-blocking system, which is the successful sexual reproduction of plants. As plant sperm cells are mediated by male–female crosstalk communication, to avoid non-motile and egg cells are embedded deep inside the female attraction of multiple pollen tubes, is also reviewed. tissues, a pollen tube delivers the two sperm cells that it contains by growing towards the ovule, in which the egg cell resides. Pollen tube KEY WORDS: Pollen tube, Sexual plant reproduction, One-to-one pollen tube guidance, Intercellular communication, Chemical growth towards the ovule is precisely controlled and divided into attractants, LUREs two stages, preovular and ovular guidance. In this Cell Science at a Glance article and accompanying poster, we provide a Introduction comprehensive overview of pollen tube guidance and highlight An efficient and successful fertilization is important to flowering some of the attractant peptides used during ovular guidance. We plants, which have limited time for fertilization and a restricted supply of water. Here, the egg cell is deeply embedded inside the ovule to avoid damage (see poster and glossary). The pollen tube of 1Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Furo- cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan. 2Precursory Research for the male gametophyte includes a vegetative nucleus and two sperm Embryonic Science and Technology (PRESTO), Japan Science and Technology cells. Sperm cells are non-motile (Berger et al., 2008), so they need Agency (JST), Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan. 3Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464- to be delivered through the pollen tube to the egg cell in the ovule 8602, Japan. (Zhang et al., 2017). The pollen tube is a polarized cell that grows at the tip in a manner that is controlled by cytoskeleton dynamics *Author for correspondence ([email protected]) (Cheung and Wu, 2008). The pollen tube grows through the pistil Y.M., 0000-0002-8086-2297 and reaches the ovule, where it invades the synergid cell and Journal of Cell Science 1 CELL SCIENCE AT A GLANCE Journal of Cell Science (2018) 131, jcs208447. doi:10.1242/jcs.208447 Glossary Double fertilization: one sperm cell fertilizes the egg cell to form the embryo and another sperm cell fertilizes the central cell to produce the endosperm (in flowering plants). Egg cell: the female reproductive cell that fuses with a male reproductive cell (sperm cell) to form the embryo. Embryo sac: a female gametophyte in flowering plants. The mature embryo sac contains two female gametes (the egg and central cell) and adjacent accessory cells (the synergid and antipodal cells). Filiform apparatus: fibrous membrane-enriched cell wall region at the micropylar end in the synergid cell. Funiculus: a stalk-like structure that connects ovules to the placenta in the ovary. Funicular guidance: a mechanism of pollen tube guidance from the surface of the septum to the funiculus. Gametophytic tissues: reproductive cells (gametes) are generated in haploid gametophytic tissues. The male gametophytic tissue is the pollen and, for the female plant, it is the embryo sac. Generative cell: see ‘vegetative nucleus’. Integument: the outer layer that surrounds the ovule in diploid female tissues. Male germ unit: an assembly of sperm cells and the vegetative nucleus, which is formed by extracellular matrix of the sperm cells and the physical association of sperm cell and the vegetative nucleus. Microgametogenesis: a reproductive process that produces a male gametophyte (pollen) in the anther of flowering plants. Micropylar guidance: a mechanism of pollen tube guidance from the funiculus to the micropyle. Micropyle: a small hole that is formed without closing the edge of the integument in the ovule. The pollen tube penetrates the embryo sac through this hole. Microspore: a spore that develops into the male gametophytes (pollen) in flowering plants. Microsporogenesis: the process by which the diploid nucleus of the microspore mother cell undergoes meiosis to form four haploid microspores. Ovary: a reproductive organ that contains the ovules to produce the seeds. Fruits are mature ovaries after fertilization. Ovule: a maternal seed tissue before fertilization in flowering plants. The ovule contains the integument and the embryo sac. Pistil: a female reproductive organ of flowering plants. The pistil contains the stigma, the style, and the ovary. Pollen: the male gametophyte of plants that contains either two sperm cells or a generative cell and a vegetative cell. Pollen tube: a protuberant and tip-growing cylindrical cell of the pollen that contains sperm cells or generative cells. Pollen tube emergence: pollen tubes emerge from the transmitting tract tissue inside the septum to the septum surface. Pollen tube rupture: the rupture that occurs when the pollen tube arrives at the synergid cells. Pollen tube discharges the two sperm cells to the egg and central cells. Semi-in vitro fertilization assay: method to co-cultivate and analyze pollen tubes and ovules on solid medium. Pollinated stigma is cut and placed on the medium, which enables observation of pollen tubes that grow from the end of the cut style to the ovule. Septum: a planar tissue between each space inside the pistil. In Arabidopsis, two carpels are fused to make spaces that contain the ovules. Stigma: the part of the pistil that receives the pollen. After the pollen is attached to the stigma, the pollen is hydrated and germinates the pollen tube, which allows penetration into the pistil. Style: a structure that connects the stigma and the ovary in the pistil of flowering plants. Synergid cells: accessory cells that are adjacent to the egg cell in the embryo sac of flowering plants. The functions of synergid cells are pollen tube attraction and reception. Transmitting tract: In Arabidopsis, the tissue that includes cylindrical cells and the extracellular matrix to form a passage for the pollen tube inside the pistil. Vegetative nucleus: the pollen tube nucleus. During microgametogenesis, the microspore divides asymmetrically to give rise to the vegetative nucleus and the generative cell through a first round of mitosis. Following a second round of mitosis, the generative cell divides into two sperm cells in the pollen or pollen tube of flowering plants. subsequently ruptures; this leads to the discharge of its cytoplasmic tube germination) before it then penetrates into the pistil tissue (Sze content, including the sperm cells, and double fertilization occurs et al., 2014). In flowering plants, pistils can be categorized as single- (see glossary) (Hamamura et al., 2011). In order to reach the ovular and multi-ovular types. Multi-ovular pistils, such as in micropyle, the opening of the ovule, precisely and quickly, a plant- Arabidopsis thaliana, enclose ∼60 ovules (Cucinotta et al., 2014). specific navigation system that is called ‘pollen tube guidance’ has Over 100 pollen tubes grow inside the pistil (Pagnussat et al., 2007). evolved. Here, and in the accompanying poster, we summarize the However, it is rare that multiple pollen tubes enter one ovule; the molecular mechanisms of pollen tube guidance and highlight its frequency is ∼2% in maize (Kato, 2001) and ∼1% in A. thaliana chemical attractant molecules. (Huck et al., 2003; Rotman et al., 2003). Therefore, ‘pollen tube guidance’ as a plant-specific navigation system is needed to One-to-one pollen tube guidance facilitate the exact one-to-one coupling between sibling ovules and In flowering plants, male microsporogenesis and numerous individual pollen tubes. microgametogenesis occur in the anther (Suzuki, 2009). Following meiosis, the microspore develops into pollen, the male Multistep control of pollen tube guidance gametophyte. Within the anther, the microspore undergoes a first Pollen tubes elongate within the pistil to find the ovule through round of mitosis, which results in the formation of two unequal cells multiple steps: (1) stigma penetration, (2) elongation into the that contain a haploid nucleus: the large vegetative cell and the small transmitting tract, (3) emergence from the transmitting tract, generative cell. The generative cell divides during pollen (4) funicular guidance, and (5) micropylar guidance (see glossary) development or pollen tube elongation in a second round of (Johnson and Lord, 2006). Pollen tubes grow through various female mitosis to form the two sperm cells (see glossary). The vegetative tissues, such as the stigma, style, transmitting tract, septum and the nucleus and two sperm cells are then transported passively in the surface of the funiculus (Cheung, 1996). The precision in pollen tube pollen tube as the male germ unit (McCue et al., 2011, see poster guidance thereby results from crosstalk between these female tissues and glossary). When pollen lands on the stigma, the pollen hydrates and the pollen tube (Vogler et al., 2016), that is incompatible pollen and this causes a protuberance of the tip of the pollen tube (pollen tubes are rejected by cell-to-cell communication between the pollen Journal of Cell Science 2 CELL SCIENCE AT A GLANCE Journal of Cell Science (2018) 131, jcs208447. doi:10.1242/jcs.208447 tubes and the female tissues (Takayama and Isogai, 2005; Chapman the solid style, as in A. thaliana (At) (Erbar, 2003; Lennon et al., and Goring, 2010; Swanson et al., 2004). These multistep controls 1998). Proteins such as NO TRANSMITTING TRACT (NTT), can be categorized into preovular and ovular guidance (Higashiyama HECATE 1 (HEC1), HEC2, HEC3, HALF FILLED (HAF), and Takeuchi, 2015; Kanaoka and Higashiyama, 2015).
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