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

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.

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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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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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Overgrowth of Pollen Tubes in Embryo Sacs of Rhododendron Following Interspecific Pollinations

Australian Journal of Botany ◽

10.1071/bt9860413 ◽

1986 ◽

Vol 34 (4) ◽

pp. 413 ◽

Cited By ~ 25

Author(s):

EG Williams ◽

V Kaul ◽

JL Rouse ◽

BF Palser

Keyword(s):

Pollen Tube ◽

Embryo Sac ◽

Pollen Tubes ◽

Egg Cell ◽

Interspecific Crosses ◽

Main Body

Frequent overgrowths of pollen tubes within the embryo sac are characteristic of a number of interspecific crosses in the genus Rhododendron (Ericaceae). The combined techniques of sectioning, squashing and whole-ovule clearing have confirmed that in ovules showing this phenomenon the pollen tube fails to terminate growth and release sperms on entry into a synergid; instead it continues to grow beyond the synergid and egg cell, often filling the main body of the embryo sac with a coiled and distorted mass. Such ovules fail to develop further. The occurrence and possible causes of this error syndrome are discussed.

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Pollen Tube Growth in Interspecific Crosses between Capsicum Species

HortScience ◽

10.21273/hortsci.26.5.585 ◽

1991 ◽

Vol 26 (5) ◽

pp. 585-586 ◽

Cited By ~ 22

Author(s):

Sierd Zijlstra ◽

Coen Purimahua ◽

Pim Lindhout

Keyword(s):

Pollen Tube ◽

Capsicum Annuum ◽

Pollen Tube Growth ◽

Pollen Tubes ◽

Tube Growth ◽

Egg Cell ◽

Interspecific Crosses ◽

Capsicum Species ◽

Pollen Tube Penetration ◽

Capsicum Chacoense

Crossing barriers between white- and purple-flowered species were examined. Four accessions of Capsicum annuum and three of C. pubescens were reciprocally crossed with one to four accessions of C. baccatum, C. cardenasii, C. chacoense, C. chinense, C. eximium, C. frutescens, C. galapagoense, and C. praetermissum. Capsicum chacoense is the only white-flowered species that inhibits C. annuum pollen tube growth but allows C. pubescens pollen tube penetration into the egg cell. Capsicum cardenasii and C. eximium exhibit similar crossabilities with C. annuum and C. pubescens: pollen tubes of C. cardenasii and of C. eximium can penetrate the egg cells of C. annuum but not vice versa, and pollen tubes of C. pubescens can penetrate the egg cells of C. cardenasii and of C. eximium but not vice versa.

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Female gametophyte-controlled pollen tube guidance

Biochemical Society Transactions ◽

10.1042/bst0380627 ◽

2010 ◽

Vol 38 (2) ◽

pp. 627-630 ◽

Cited By ~ 37

Author(s):

Mihaela-Luiza Márton ◽

Thomas Dresselhaus

Keyword(s):

Pollen Tube ◽

Female Gametophyte ◽

Cell Communication ◽

Flowering Plants ◽

Sperm Cells ◽

Double Fertilization ◽

Pollen Tube Guidance ◽

Communication Events ◽

Extensive Cell

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.

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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.

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CrRLK1L receptor-like kinases HERCULES RECEPTOR KINASE 1 and ANJEA are female determinants of pollen tube reception

10.1101/428854 ◽

2018 ◽

Author(s):

Sergio Galindo-Trigo ◽

Noel Blanco-Touriñán ◽

Thomas A. DeFalco ◽

Eloise S. Wells ◽

Julie E Gray ◽

...

Keyword(s):

Pollen Tube ◽

Female Gametophyte ◽

Male Gametophyte ◽

Oxygen Species ◽

Receptor Kinase ◽

In Planta ◽

Filiform Apparatus ◽

Synergid Cell ◽

Receptor Kinases ◽

Type Receptor

AbstractCommunication between the gametophytes is vital for angiosperm fertilisation. Multiple CrRLK1L-type receptor kinases prevent premature pollen tube burst, while another CrRLK1L protein, FERONIA (FER), is required for pollen tube burst in the female gametophyte. We report here the identification of two additional CrRLK1L homologues, HERCULES RECEPTOR KINASE 1 (HERK1) and ANJEA (ANJ), which act redundantly to promote pollen tube burst at the synergid cells. HERK1 and ANJ localise to the filiform apparatus of the synergid cells in unfertilised ovules, and in herk1 anj mutants a majority of ovules remain unfertilised due to pollen tube overgrowth, together indicating that HERK1 and ANJ act as female determinants for fertilisation. As in fer mutants, the synergid cell-specific, endomembrane protein NORTIA (NTA) is not relocalised after pollen tube reception; however, unlike fer mutants, reactive oxygen species levels are unaffected in herk1 anj double mutants. Both ANJ and HERK1 associate with FER and its proposed co-receptor LORELEI (LRE) in planta. Together, our data indicate that HERK1 and ANJ act with FER to mediate female-male gametophyte interactions during plant fertilisation.

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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.

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