Female gametophyte-controlled pollen tube guidance

During the evolution of flowering plants, their sperm cells have lost mobility and are transported from the stigma to the female gametophyte via the pollen tube to achieve double fertilization. Pollen tube growth and guidance is largely governed by the maternal sporophytic tissues of the stigma, style and ovule. However, the last phase of the pollen tube path is under female gametophyte control and is expected to require extensive cell–cell communication events between both gametophytes. Until recently, little was known about the molecules produced by the female gametophyte that are involved in this process. In the present paper, we review the most recent development in this field and focus on the role of secreted candidate signalling ligands.

Download Full-text

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.

Download Full-text

Spatio-Temporal Distribution of Cell Wall Components in the Placentas, Ovules and Female Gametophytes of Utricularia during Pollination

International Journal of Molecular Sciences ◽

10.3390/ijms22115622 ◽

2021 ◽

Vol 22 (11) ◽

pp. 5622

Author(s):

Bartosz Jan Płachno ◽

Małgorzata Kapusta ◽

Piotr Świątek ◽

Krzysztof Banaś ◽

Vitor F. O. Miranda ◽

...

Keyword(s):

Pollen Tube ◽

Female Gametophyte ◽

Embryo Sac ◽

Temporal Distribution ◽

Arabinogalactan Proteins ◽

Central Cell ◽

Nutritive Tissue ◽

Pollen Tube Guidance ◽

Micropylar Canal

In most angiosperms, the female gametophyte is hidden in the mother tissues and the pollen tube enters the ovule via a micropylar canal. The mother tissues play an essential role in the pollen tube guidance. However, in Utricularia, the female gametophyte surpasses the entire micropylar canal and extends beyond the limit of the integument. The female gametophyte then invades the placenta and a part of the central cell has direct contact with the ovary chamber. To date, information about the role of the placenta and integument in pollen tube guidance in Utricularia, which have extra-ovular female gametophytes, has been lacking. The aim of this study was to evaluate the role of the placenta, central cell and integument in pollen tube pollen tube guidance in Utricularia nelumbifolia Gardner and Utricularia humboldtii R.H. Schomb. by studying the production of arabinogalactan proteins. It was also determined whether the production of the arabinogalactan proteins is dependent on pollination in Utricularia. In both of the examined species, arabinogalactan proteins (AGPs) were observed in the placenta (epidermis and nutritive tissue), ovule (integument, chalaza), and female gametophyte of both pollinated and unpollinated flowers, which means that the production of AGPs is independent of pollination; however, the production of some AGPs was lower after fertilization. There were some differences in the production of AGPs between the examined species. The occurrence of AGPs in the placental epidermis and nutritive tissue suggests that they function as an obturator. The production of some AGPs in the ovular tissues (nucellus, integument) was independent of the presence of a mature embryo sac.

Download Full-text

Interactions between pollen tube and pistil control pollen tube identity and sperm release in the Arabidopsis female gametophyte

Biochemical Society Transactions ◽

10.1042/bst20130223 ◽

2014 ◽

Vol 42 (2) ◽

pp. 340-345 ◽

Cited By ~ 13

Author(s):

Alexander R. Leydon ◽

Adisorn Chaibang ◽

Mark A. Johnson

Keyword(s):

Pollen Tube ◽

Female Gametophyte ◽

Flowering Plants ◽

Flowering Plant ◽

Pollen Tube Guidance ◽

Pollen Cell ◽

Its Gene ◽

Flowering Plant Species ◽

Arabidopsis Pollen ◽

Signalling Systems

Flowering plants have immotile sperm that develop within the pollen cytoplasm and are delivered to female gametes by a pollen tube, a highly polarized extension of the pollen cell. In many flowering plant species, including seed crop plants, hundreds of pollen tubes grow towards a limited number of ovules. This system should ensure maximal fertilization of ovules and seed production; however, we know very little about how signalling between the critical cells is integrated to orchestrate delivery of two functional sperm to each ovule. Recent studies suggest that the pollen tube changes its gene-expression programme in response to growth through pistil tissue and that this differentiation process is critical for pollen tube attraction by the female gametophyte and for release of sperm. Interestingly, these two signalling systems, called pollen tube guidance and pollen tube reception, are also species-preferential. The present review focuses on Arabidopsis pollen tube differentiation within the pistil and addresses the idea that pollen tube differentiation defines pollen tube identity and recognition by female cells. We review recent identification of genes that may control pollen tube–female gametophyte recognition and discuss how these may be involved in blocking interspecific hybridization.

Download Full-text

The role of the integuments in pollen tube guidance in flowering plants

New Phytologist ◽

10.1111/nph.15420 ◽

2018 ◽

Vol 221 (2) ◽

pp. 1074-1089 ◽

Cited By ~ 4

Author(s):

Jorge Lora ◽

Thomas Laux ◽

José I. Hormaza

Keyword(s):

Pollen Tube ◽

Flowering Plants ◽

Pollen Tube Guidance

Download Full-text

Pollen tube contents initiate ovule enlargement and enhance seed coat development without fertilization

Science Advances ◽

10.1126/sciadv.1600554 ◽

2016 ◽

Vol 2 (10) ◽

pp. e1600554 ◽

Cited By ~ 19

Author(s):

Ryushiro D. Kasahara ◽

Michitaka Notaguchi ◽

Shiori Nagahara ◽

Takamasa Suzuki ◽

Daichi Susaki ◽

...

Keyword(s):

Pollen Tube ◽

Seminal Plasma ◽

Vital Role ◽

Sperm Cells ◽

Double Fertilization ◽

Seed Formation ◽

Pollen Tube Guidance ◽

Tube Content ◽

Endosperm Mutants ◽

Autonomous Endosperm

In angiosperms, pollen tubes carry two sperm cells toward the egg and central cells to complete double fertilization. In animals, not only sperm but also seminal plasma is required for proper fertilization. However, little is known regarding the function of pollen tube content (PTC), which is analogous to seminal plasma. We report that the PTC plays a vital role in the prefertilization state and causes an enlargement of ovules without fertilization. We termed this phenomenon as pollen tube–dependent ovule enlargement morphology and placed it between pollen tube guidance and double fertilization. Additionally, PTC increases endosperm nuclei without fertilization when combined with autonomous endosperm mutants. This finding could be applied in agriculture, particularly in enhancing seed formation without fertilization in important crops.

Download Full-text

The Long Journey of Pollen Tube in the Pistil

International Journal of Molecular Sciences ◽

10.3390/ijms19113529 ◽

2018 ◽

Vol 19 (11) ◽

pp. 3529 ◽

Cited By ~ 13

Author(s):

Yang-Yang Zheng ◽

Xian-Ju Lin ◽

Hui-Min Liang ◽

Fang-Fei Wang ◽

Li-Yu Chen

Keyword(s):

Pollen Tube ◽

Female Gametophyte ◽

Male Gametophyte ◽

Pollen Grain ◽

Tubular Structure ◽

Future Research ◽

Sperm Cells ◽

Double Fertilization ◽

Complex Process ◽

Pass Through

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.

Download Full-text

Female gametophyte expressed Arabidopsis thaliana lipid transfer proteins AtLtpI.4 and AtLtpI.8 provide a link between callose homeostasis, pollen tube guidance, and fertilization success

10.1101/2021.01.13.426551 ◽

2021 ◽

Author(s):

Khushbu Kumari ◽

Meng Zhao ◽

Sebastian Britz ◽

Christine Weiste ◽

Wolfgang Dröge-Laser ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Pollen Tube ◽

Female Gametophyte ◽

Control Cell ◽

Cell Communication ◽

Large Family ◽

Fertilization Success ◽

Lipid Transfer ◽

Lipid Transfer Proteins ◽

Pollen Tube Guidance

ABSTRACTNon-specific lipid transfer proteins (LTPs) represent a sub-class among the large family of Cysteine-rich proteins (CRPs) specific to land plants. LTPs possess a hydrophobic cavity, enabling them to bind and stabilize a variety of lipid molecules outside membranes. In line with the existence of an N-terminal signal peptide, secreted LTPs represent a well-suited mobile signal carrier in the plant’s extracellular matrix. Thus, LTPs are currently considered as key players to mediate the bulk flow of lipids between membranes/compartments as well as the buildup of lipid barrier polymers including cutin and suberin.Here, we show that floral expressed Arabidopsis thaliana AtLtpI.4 (AtLTP2) and AtLtpI.8 (AtLTP5), mutually control cell-cell communication between growing pollen tubes and ovules during fertilization. Arabidopsis mutants lacking functional AtLtpI.4 and AtLtpI.8 exhibit significantly reduced fertilization success. Cross-pollination and cell biological analyses revealed that AtLtpI.4/I.8 double mutants are impaired in pollen tube guidance towards ovules. Our finding that the AtLtpI.4/I.8 phenotype correlates with aberrant callose depositions in the micropylar region during ovule development suggests that both LTPs represent novel players of a joint signaling pathway that controls callose homeostasis in the female gametophyte.

Download Full-text

Pollination in Arabidopsis Thaliana

Microscopy and Microanalysis ◽

10.1017/s1431927600026027 ◽

1998 ◽

Vol 4 (S2) ◽

pp. 1180-1181

Author(s):

K. Lennon ◽

E. Lord

Keyword(s):

Pollen Tube ◽

Cell Communication ◽

Embryo Sac ◽

Pollen Grain ◽

Secretory Cells ◽

Higher Plant ◽

Transmitting Tissue ◽

Pollen Tube Guidance ◽

Complex Processes ◽

Communication Events

In flowering plants, pollination and the process of fertilization are complex processes involving a series of cell-to-cell communication events. Though details of the progression of the pollen tube through the pistil, beginning with germination of the pollen grain on the stigma and culminating with delivery of the sperm cells to the embryo sac, are well established for several higher plant species, the mechanisms involved have yet to be elucidated. It has been shown that the transmitting tissue, which coincides with the path of pollen tubes in the gynoecium, is composed of highly secretory cells characterized by an extensive extracellular matrix (ECM). The actual roles that this ECM plays in pollination are currently unknown, although functions proposed include mechanical and/or chemotropic pollen tube guidance as well as pollen tube nutrition.

Download Full-text

Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance

Development ◽

10.1242/dev.127.20.4511 ◽

2000 ◽

Vol 127 (20) ◽

pp. 4511-4518 ◽

Cited By ~ 2

Author(s):

K.K. Shimizu ◽

K. Okada

Keyword(s):

Pollen Tube ◽

Female Gametophyte ◽

Inclusive Fitness ◽

Male Gametophyte ◽

Pollen Tubes ◽

Interspecific Crosses ◽

Pollen Tube Guidance ◽

Normal Number ◽

Mutant Female ◽

Diploid Cells

Sexual reproduction in plants, unlike that of animals, requires the action of multicellular haploid gametophytes. The male gametophyte (pollen tube) is guided to a female gametophyte through diploid sporophytic cells in the pistil. While interactions between the pollen tube and diploid cells have been described, little is known about the intercellular recognition systems between the pollen tube and the female gametophyte. In particular, the mechanisms that enable only one pollen tube to interact with each female gametophyte, thereby preventing polysperm, are not understood. We isolated female gametophyte mutants named magatama (maa) from Arabidopsis thaliana by screening for siliques containing half the normal number of mature seeds. In maa1 and maa3 mutants, in which the development of the female gametophyte was delayed, pollen tube guidance was affected. Pollen tubes were directed to mutant female gametophytes, but they lost their way just before entering the micropyle and elongated in random directions. Moreover, the mutant female gametophytes attracted two pollen tubes at a high frequency. To explain the interaction between gametophytes, we propose a monogamy model in which a female gametophyte emits two attractants and prevents polyspermy. This prevention process by the female gametophyte could increase a plant's inclusive fitness by facilitating the fertilization of sibling female gametophytes. In addition, repulsion between pollen tubes might help prevent polyspermy. The reproductive isolations observed in interspecific crosses in Brassicaceae are also consistent with the monogamy model.

Download Full-text

Reproductive Multitasking: The Female Gametophyte

Annual Review of Plant Biology ◽

10.1146/annurev-arplant-081519-035943 ◽

2020 ◽

Vol 71 (1) ◽

pp. 517-546 ◽

Cited By ~ 1

Author(s):

Friederike Hater ◽

Thomas Nakel ◽

Rita Groß-Hardt

Keyword(s):

Pollen Tube ◽

Female Gametophyte ◽

Flowering Plants ◽

Molecular Control ◽

Repair Mechanisms ◽

Plant Hybridization ◽

Evolutionary Success ◽

Underlying Mechanisms ◽

And Function ◽

Functional Megaspore

Fertilization of flowering plants requires the organization of complex tasks, many of which become integrated by the female gametophyte (FG). The FG is a few-celled haploid structure that orchestrates division of labor to coordinate successful interaction with the sperm cells and their transport vehicle, the pollen tube. As reproductive outcome is directly coupled to evolutionary success, the underlying mechanisms are under robust molecular control, including integrity check and repair mechanisms. Here, we review progress on understanding the development and function of the FG, starting with the functional megaspore, which represents the haploid founder cell of the FG. We highlight recent achievements that have greatly advanced our understanding of pollen tube attraction strategies and the mechanisms that regulate plant hybridization and gamete fusion. In addition, we discuss novel insights into plant polyploidization strategies that expand current concepts on the evolution of flowering plants.

Download Full-text