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The Long Journey of Pollen Tube in the Pistil

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The Long Journey of Pollen Tube in the Pistil International Journal of Molecular Sciences Review The Long Journey of Pollen Tube in the Pistil Yang-Yang Zheng 1,†, Xian-Ju Lin 1,† , Hui-Min Liang 1, Fang-Fei Wang 2 and Li-Yu Chen 1,* 1 Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Center for Genomics and Biotechnology, School of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, China; [email protected] (Y.-Y.Z.); [email protected] (X.-J.L.); [email protected] (H.-M.L.) 2 State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China; [email protected] * Correspondence: [email protected] † These authors contributed equally to this work. Received: 30 September 2018; Accepted: 7 November 2018; Published: 9 November 2018 Abstract: In non-cleistogamous plants, the male gametophyte, the pollen grain is immotile and exploits various agents, such as pollinators, wind, and even water, to arrive to a receptive stigma. The complex process of pollination involves a tubular structure, i.e., the pollen tube, which delivers the two sperm cells to the female gametophyte to enable double fertilization. The pollen tube has to penetrate the stigma, grow in the style tissues, pass through the septum, grow along the funiculus, and navigate to the micropyle of the ovule. It is a long journey for the pollen tube and its two sperm cells before they meet the female gametophyte, and it requires very accurate regulation to perform successful fertilization. In this review, we update the knowledge of molecular dialogues of pollen-pistil interaction, especially the progress of pollen tube activation and guidance, and give perspectives for future research. Keywords: female gametophyte; male gametophyte; pollen tube guidance; sexual reproduction; stigma; transmitting tract 1. Introduction Successful pollination and fertilization are crucial for sexual plant reproduction in flowering plants. The entire pollination and fertilization process consists of a number of successive steps initiated after pollen landing on the stigma, and its adhesion, hydration, and germination to produce a pollen tube. The pollen tube grows through the style, and then enters into the transmitting tract. It will be attracted by the signals from the ovule [1], and emerge onto the septum, and grow along the funiculus, navigating to the micropyle of the ovule (Figure1). During pollen tube growth, sperm cells move within the pollen tube, and once the pollen tube reaches the female gametophyte, the two sperms will be released and fuse with the egg cell and the central cell, respectively, for double fertilization. It is a long journey for the pollen tube and its valuable passengers, two sperm cells. There are lots of cell-cell signaling and other interactions involved in these complicated processes. In the past three decades, we have progressed in our understanding of the molecular regulation of the pollen tube journey following the huge advances in plant genetics, genomics, and molecular biology, as well as following the use of model plants. Here, we review the progress of molecular regulation of pollen-pistil interaction. Int. J. Mol. Sci. 2018, 19, 3529; doi:10.3390/ijms19113529 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2018, 19, 3529 2 of 15 Int. J. Mol. Sci. 2018, 19, x FOR PEER REVIEW 2 of 14 Figure 1. Pollen tube growth in the pistil. (a) Schematic diagram of pollen grains that land on the Figure 1. Pollen tube growth in the pistil. (a) Schematic diagram of pollen grains that land on the stigma and germinate to produce pollen tubes that grow within the pistil. (b) Arabidopsis thaliana pollen stigma and germinate to produce pollen tubes that grow within the pistil. (b) Arabidopsis thaliana tubes in a pistil, stained by aniline blue. The image was observed under Olympus BX63 automatic pollen tubes in a pistil, stained by aniline blue. The image was observed under Olympus BX63 fluorescence microscope. Scale bar = 100 µm. automatic fluorescence microscope. Scale bar = 100 μm. 2. Pollen Adhesion and Recognition 2. Pollen Adhesion and Recognition Once the pollen grains, released from the anther, arrive to the stigma’s surface, they form productiveOnce the contacts pollen with grains, the pistilreleased tissues. from Different the anther from, arrive the intercellular to the stigma’s contacts surface, thatparticipate they form inproductive animal cells, contacts these with interactions the pistil take tissues. place Different between from cells the with intercellular cell walls and contacts with theirthat participate extracellular in matrices.animal cells, The these mature interactions pollen cell take wall place includes between three cells mainwith layerscell walls with and some with variation their extracellular between differentmatrices. species:The mature (1) A pollen coatcell thatwall fillsincludes the empty three cavitiesmain layers of the with exine, some and therevariation are aromaticbetween compounds,different species: lipids, (1) pigments,A pollen coat and that proteins fills the within empty it; cavities (2) an outerof the strataexine, (exineand there wall), are whicharomatic is multilayered,compounds, lipids, composed pigments, of sporopollenin, and proteins and within broken it; (2) by gapsan outer called strata apertures; (exine wall), (3) an which internal is stratamultilayered, (the intine) composed primarily of sporopolle made of pectinnin, and and broken cellulose by gaps [2]. called On the apertures; basis of the(3) an character internal of strata the extracellular(the intine) primarily matrix that made covers of pectin their and surface, cellulose stigmas [2]. On are the generallybasis of the divided character into of the two extracellular categories: Wetmatrix stigmas that covers coated withtheir viscoussurface, secretionsstigmas are are ge foundnerally in divided various families,into two includingcategories: Leguminosae, Wet stigmas Solanaceae,coated with andviscous Orchidaceae, secretions andare found pollen in tends variou tos befamilies, captured including and hydrate Leguminosae, nonspecifically Solanaceae, on wetand stigmas;Orchidaceae, dry stigmas and pollen found tends in families, to be suchcaptured as Asteraceae, and hydrate Gramineae, nonspecifically and Brassicaceae, on wet stigmas; are coated dry withstigmas a proteinic found in pellicle families, [3]. such Because as Asteraceae, of the surface Gramineae, barriers responsibleand Brassicaceae, for hampering are coated pathogen with a infections,proteinic pellicle dry stigmas [3]. Because tightly regulateof the surface the adopting barriers of responsible pollen [3]. for In thehampering Brassicaceae, pathogen which infections, includes thedry model stigmas plant, tightlyArabidopsis regulate thalianathe adopting, dry stigmas of pollen are [3]. coated In the with Brassicaceae, papillae cells, which which includes act as the the model first pointplant, of Arabidopsis contact with thaliana pollen, dry during stigmas pollen-pistil are coated interactions. with papillae cells, which act as the first point of contactSelf-incompatibility with pollen during (SI) pollen-pistil is one of the interactions. most important systems to preventing inbreeding in many floweringSelf-incompatibility plants. Based on(SI) genetic is one of studies, the most SI canimportant be classified systems into to preventing two systems, inbreeding gametophytic in many SI (GSI)flowering and sporophyticplants. Based SI on (SSI), genetic which studies, are distinguished SI can be classified by the geneticinto two behavior systems, of gametophytic the pollen’s SISI phenotype(GSI) and sporophytic [4]. In the Brassicaceae, SI (SSI), which SSI will are occurdistinguis rapidlyhed during by the pollen genetic adhesion behavior to of the the stigma pollen’s [5]. SI phenotypeOn account [4]. In of the the Brassicaceae, variety of pollen SSI will coats occur and stigmarapidly exudates,during pollen the pollen-stigma adhesion to the interface stigma is [5]. also highlyOn variable. account Inof the self-compatible variety of pollenArabidopsis coats and, it stigma is proven exudates, that the the property pollen-stigma of the interface pollen-stigma is also interfacehighly variable. alters during In self-compatible pollination progresses, Arabidopsis becoming, it is proven fairly that tougher the overproperty time, of with the different pollen-stigma kinds ofinterface adhesive alters interactions during pollination supplanting progresses, and replenishing becoming each fairly other toughe [6]. Pollenr over grains time, with adhere different to their kinds own stigmaof adhesive with highinteractions affinity; whilesupplanti theyng bind and stigmas replenishing from other each botanic other families[6]. Pollen poorly, grains even adhere stigmas to fromtheir relevantown stigmaBrassica withspecies, high affinity; indicating while a species-specific they bind stigmas manner from that other lower botanic improper families pollen poorly, access even [6]. stigmas from relevant Brassica species, indicating a species-specific manner that lower improper pollen access [6]. A very rapid “original” adhesion step was measured that depends on the pollen Int. J. Mol. Sci. 2018, 19, 3529 3 of 15 A very rapid “original” adhesion step was measured that depends on the pollen exine, but not on the pollen coat [6]. The pollen coat is mobilized
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