Signaling at Physical Barriers during Pollen–Pistil Interactions

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.

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Functional genomics of pollen tube–pistil interactions in Arabidopsis

Biochemical Society Transactions ◽

10.1042/bst0380593 ◽

2010 ◽

Vol 38 (2) ◽

pp. 593-597 ◽

Cited By ~ 17

Author(s):

Ravishankar Palanivelu ◽

Mark A. Johnson

Keyword(s):

Pollen Tube ◽

Regulatory Networks ◽

Genomic Analysis ◽

Pollen Tubes ◽

Cellular Growth ◽

Functional Genomic ◽

Reverse Genetic ◽

Guidance Cues ◽

Functional Genomic Analysis

The pollen tube represents an attractive model system for functional genomic analysis of the cell–cell interactions that mediate guided cellular growth. The pollen tube extends through pistil tissues and responds to guidance cues that direct the tube towards an ovule, where it releases sperm for fertilization. Pollen is readily isolated from anthers, where it is produced, and can be induced to produce a tube in vitro. Interestingly, pollen tube growth is significantly enhanced in pistils, and pollen tubes are rendered competent to respond to guidance cues after growth in a pistil. This potentiation of the pollen tube by the pistil suggested that pollen tubes alter their gene-expression programme in response to their environment. Recently, the transcriptomes of pollen tubes grown in vitro or through pistil tissues were determined. Significant changes in the transcriptome were found to accompany growth in vitro and through the pistil tissues. Reverse genetic analysis of pollen-tube-induced genes identified a new set of factors critical for pollen tube extension and navigation of the pistil environment. Recent advances reviewed in the present paper suggest that functional genomic analysis of pollen tubes has the potential to uncover the regulatory networks that shape the genetic architecture of the pollen tube as it responds to migratory cues produced by the pistil.

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Pollen tube guidance by the female gametophyte

Development ◽

10.1242/dev.124.12.2489 ◽

1997 ◽

Vol 124 (12) ◽

pp. 2489-2498 ◽

Cited By ~ 1

Author(s):

S.M. Ray ◽

S.S. Park ◽

A. Ray

Keyword(s):

Pollen Tube ◽

Long Range ◽

Female Gametophyte ◽

Chromosomal Translocation ◽

Pollen Grains ◽

Pollen Tubes ◽

Flowering Plants ◽

Genetic Studies ◽

Transmitting Tract ◽

Pollen Tube Guidance

In flowering plants, pollen grains germinate on the pistil and send pollen tubes down the transmitting tract toward ovules. Previous genetic studies suggested that the ovule is responsible for long-range pollen tube guidance during the last phase of a pollen tube's journey to the female gametes. It was not possible, however, to unambiguously identify the signaling cells within an ovule: the haploid female gametophyte or the diploid sporophytic cells. In an effort to distinguish genetically between these two possibilities, we have used a reciprocal chromosomal translocation to generate flowers wherein approximately half the ovules do not contain a functional female gametophyte but all ovules contain genotypically normal sporophytic cells. In these flowers, pollen tubes are guided to the normal but not to the abnormal female gametophytes. These results strongly suggest that the female gametophyte is responsible for pollen tube guidance, but leave open the possibility that the gametophyte may accomplish this indirectly through its influence on some sporophytic cells.

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The RSS system of unidirectional cross-incompatibility in maize. 2. Cytology

Genome ◽

10.1139/g92-083 ◽

1992 ◽

Vol 35 (4) ◽

pp. 560-564

Author(s):

Abdul Rashid ◽

Peter A. Peterson

Keyword(s):

Pollen Tube ◽

Female Parent ◽

Pollen Tubes ◽

Pollen Grain ◽

Maize Pollen ◽

Transmitting Tract ◽

Incompatible Pollination ◽

Recessive Genes ◽

Maize Genetics ◽

Incompatibility Reaction

In 1975, a number of genetic lines discovered in our maize genetics nursery in Ames, Iowa, showed unidirectional cross-incompatibility. Later, it was found that this unidirectional cross-incompatibility is controlled by three recessive genes. One locus (cif) controls the incompatibility reaction in the female tissue and the other two (cim1 and cim2) control the incompatibility reaction in the pollen grain. The cross is incompatible only when the female parent is homozygous recessive for the cif and the male parent is homozygously recessive for the cim1 as well as the cim2 locus. Cytological studies of this unidirectional cross-incompatibility show that the site of the incompatibility reaction occurs after the entry of the pollen tubes into the transmitting tract of the incompatible silks. Between 12 and 24 h after pollination, the incompatible pollination is characterized by the swelling and bursting of pollen tubes at the tip, after which pollen tube growth stops.Key words: maize, pollen tube, cross-incompatibility.

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Reproductive Isolation and Morphogenetic Evolution in Drosophila Analyzed by Breakage of Ethological Barriers

Genetics ◽

10.1093/genetics/147.1.231 ◽

1997 ◽

Vol 147 (1) ◽

pp. 231-242 ◽

Cited By ~ 1

Author(s):

Lucas Sánchez ◽

Pedro Santamaria

Keyword(s):

Reproductive Isolation ◽

Germ Cells ◽

Morphological Analysis ◽

Seminal Fluid ◽

Germ Line ◽

Regulatory Gene ◽

Motile Sperm ◽

Male And Female ◽

Drosophila Yakuba

Abstract This article reports the breaking of ethological barriers through the constitution of soma-germ line chimeras between species of the melanogaster subgroup of Drosophila, which are ethologically isolated. Female Drosophila yakuba and D. teissieri germ cells in a D. melanogaster ovary produced functional oocytes that, when fertilized by D. melanogaster sperm, gave rise to sterile yakuba-melanogaster andteissieri-melanogaster male and female hybrids. However, the erecta-melanogaster and orena-melanogaster hybrids were lethal, since female D. erecta and D. orena germ cells in a D. melanogaster ovary failed to form oocytes with the capacity to develop normally. This failure appears to be caused by an altered interaction between the melanogaster soma and the erecta and orena germ lines. Germ cells of D. teissieri and D. orena in a D. melanogaster testis produced motile sperm that was not stored in D. melanogaster females. This might be due to incompatibility between the teissieri and orena sperm and the melanogaster seminal fluid. A morphological analysis of the terminalia of yakuba-melanogaster and teissieri-melanogaster hybrids was performed. The effect on the terminalia of teissieri-melanogaster hybrids of a mutation in doublesex, a regulatory gene that controls the development of the terminalia, was also investigated.

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Protein Analysis of Pollen Tubes after the Treatments of Membrane Trafficking Inhibitors Gains Insights on Molecular Mechanism Underlying Pollen Tube Polar Growth

The Protein Journal ◽

10.1007/s10930-021-09972-x ◽

2021 ◽

Vol 40 (2) ◽

pp. 205-222

Author(s):

Monica Scali ◽

Alessandra Moscatelli ◽

Luca Bini ◽

Elisabetta Onelli ◽

Rita Vignani ◽

...

Keyword(s):

Pollen Tube ◽

Actin Cytoskeleton ◽

Membrane Trafficking ◽

Tip Growth ◽

Male Gametophyte ◽

Pollen Tubes ◽

Structural Features ◽

Two Dimensional Gel Electrophoresis ◽

Depth Analysis

AbstractPollen tube elongation is characterized by a highly-polarized tip growth process dependent on an efficient vesicular transport system and largely mobilized by actin cytoskeleton. Pollen tubes are an ideal model system to study exocytosis, endocytosis, membrane recycling, and signaling network coordinating cellular processes, structural organization and vesicular trafficking activities required for tip growth. Proteomic analysis was applied to identifyNicotiana tabacumDifferentially Abundant Proteins (DAPs) after in vitro pollen tube treatment with membrane trafficking inhibitors Brefeldin A, Ikarugamycin and Wortmannin. Among roughly 360 proteins separated in two-dimensional gel electrophoresis, a total of 40 spots visibly changing between treated and control samples were identified by MALDI-TOF MS and LC–ESI–MS/MS analysis. The identified proteins were classified according to biological processes, and most proteins were related to pollen tube energy metabolism, including ammino acid synthesis and lipid metabolism, structural features of pollen tube growth as well modification and actin cytoskeleton organization, stress response, and protein degradation. In-depth analysis of proteins corresponding to energy-related pathways revealed the male gametophyte to be a reliable model of energy reservoir and dynamics.

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Hyperoside promotes pollen tube growth by regulating the depolymerization effect of actin-depolymerizing factor 1 on microfilaments in okra

Horticulture Research ◽

10.1038/s41438-021-00578-z ◽

2021 ◽

Vol 8 (1) ◽

Author(s):

Biying Dong ◽

Qing Yang ◽

Zhihua Song ◽

Lili Niu ◽

Hongyan Cao ◽

...

Keyword(s):

Pollen Tube ◽

Pollen Tube Growth ◽

Pollen Germination ◽

Pollen Tubes ◽

Tube Growth ◽

Actin Depolymerizing Factor ◽

Specific Mechanism ◽

Promoting Effect ◽

New Research

AbstractMature pollen germinates rapidly on the stigma, extending its pollen tube to deliver sperm cells to the ovule for fertilization. The success of this process is an important factor that limits output. The flavonoid content increased significantly during pollen germination and pollen tube growth, which suggests it may play an important role in these processes. However, the specific mechanism of this involvement has been little researched. Our previous research found that hyperoside can prolong the flowering period of Abelmoschus esculentus (okra), but its specific mechanism is still unclear. Therefore, in this study, we focused on the effect of hyperoside in regulating the actin-depolymerizing factor (ADF), which further affects the germination and growth of pollen. We found that hyperoside can prolong the effective pollination period of okra by 2–3-fold and promote the growth of pollen tubes in the style. Then, we used Nicotiana benthamiana cells as a research system and found that hyperoside accelerates the depolymerization of intercellular microfilaments. Hyperoside can promote pollen germination and pollen tube elongation in vitro. Moreover, AeADF1 was identified out of all AeADF genes as being highly expressed in pollen tubes in response to hyperoside. In addition, hyperoside promoted AeADF1-mediated microfilament dissipation according to microfilament severing experiments in vitro. In the pollen tube, the gene expression of AeADF1 was reduced to 1/5 by oligonucleotide transfection. The decrease in the expression level of AeADF1 partially reduced the promoting effect of hyperoside on pollen germination and pollen tube growth. This research provides new research directions for flavonoids in reproductive development.

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Testing of self-(in)compatibility in apricot cultivars from European breeding programmes

Horticultural Science ◽

10.17221/219/2012-hortsci ◽

2013 ◽

Vol 40 (No. 2) ◽

pp. 65-71 ◽

Cited By ~ 3

Author(s):

D. Milatović ◽

D. Nikolić ◽

B. Krška

Keyword(s):

Fluorescence Microscopy ◽

Pollen Tube ◽

Pollen Tube Growth ◽

Reliable Method ◽

Pollen Tubes ◽

Tube Growth ◽

Self Incompatibility ◽

Breeding Programmes

Self-(in)compatibility was tested in 40 new apricot cultivars from European breeding programmes. Pollen-tube growth in pistils from laboratory pollinations was analysed using the fluorescence microscopy. Cultivars were considered self-compatible if at least one pollen tube reached the ovary in the majority of pistils. Cultivars were considered self- incompatible if the growth of pollen tubes in the style stopped along with formation of characteristic swellings. Of the examined cultivars, 18 were self-compatible and 22 were self-incompatible. Fluorescence microscopy provides a relatively rapid and reliable method to determine self-incompatibility in apricot cultivars.      

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Paving the Way for Fertilization: The Role of the Transmitting Tract

International Journal of Molecular Sciences ◽

10.3390/ijms22052603 ◽

2021 ◽

Vol 22 (5) ◽

pp. 2603

Author(s):

Ana Marta Pereira ◽

Diana Moreira ◽

Sílvia Coimbra ◽

Simona Masiero

Keyword(s):

Pollen Tube ◽

Pollen Tube Growth ◽

Current Knowledge ◽

Embryo Sac ◽

Tube Growth ◽

Signaling Cascades ◽

Secretory Cells ◽

Transmitting Tract ◽

Specialized Tissue

Angiosperm reproduction relies on the precise growth of the pollen tube through different pistil tissues carrying two sperm cells into the ovules’ embryo sac, where they fuse with the egg and the central cell to accomplish double fertilization and ultimately initiate seed development. A network of intrinsic and tightly regulated communication and signaling cascades, which mediate continuous interactions between the pollen tube and the sporophytic and gametophytic female tissues, ensures the fast and meticulous growth of pollen tubes along the pistil, until it reaches the ovule embryo sac. Most of the pollen tube growth occurs in a specialized tissue—the transmitting tract—connecting the stigma, the style, and the ovary. This tissue is composed of highly secretory cells responsible for producing an extensive extracellular matrix. This multifaceted matrix is proposed to support and provide nutrition and adhesion for pollen tube growth and guidance. Insights pertaining to the mechanisms that underlie these processes remain sparse due to the difficulty of accessing and manipulating the female sporophytic tissues enclosed in the pistil. Here, we summarize the current knowledge on this key step of reproduction in flowering plants with special emphasis on the female transmitting tract tissue.

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Persistent directional growth capability in Arabidopsis thaliana pollen tubes after nuclear elimination from the apex

Nature Communications ◽

10.1038/s41467-021-22661-8 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Kazuki Motomura ◽

Hidenori Takeuchi ◽

Michitaka Notaguchi ◽

Haruna Tsuchi ◽

Atsushi Takeda ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Pollen Tube ◽

Sperm Cell ◽

Pollen Tubes ◽

Vegetative Nucleus ◽

Sperm Cells ◽

Apical Region ◽

Basal Region ◽

Specific Expression ◽

Directional Growth

AbstractDuring the double fertilization process, pollen tubes deliver two sperm cells to an ovule containing the female gametes. In the pollen tube, the vegetative nucleus and sperm cells move together to the apical region where the vegetative nucleus is thought to play a crucial role in controlling the direction and growth of the pollen tube. Here, we report the generation of pollen tubes in Arabidopsis thaliana whose vegetative nucleus and sperm cells are isolated and sealed by callose plugs in the basal region due to apical transport defects induced by mutations in the WPP domain-interacting tail-anchored proteins (WITs) and sperm cell-specific expression of a dominant mutant of the CALLOSE SYNTHASE 3 protein. Through pollen-tube guidance assays, we show that the physiologically anuclear mutant pollen tubes maintain the ability to grow and enter ovules. Our findings provide insight into the sperm cell delivery mechanism and illustrate the independence of the tip-localized vegetative nucleus from directional growth control of the pollen tube.

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