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Frontiers in Plant Science 2020The growing pollen tube has become one of the most fascinating model cell systems for investigations into cell polarity and polar cell growth in plants. Rapidly growing... (Review)
Review
The growing pollen tube has become one of the most fascinating model cell systems for investigations into cell polarity and polar cell growth in plants. Rapidly growing pollen tubes achieve tip-focused cell expansion by vigorous anterograde exocytosis, through which various newly synthesized macromolecules are directionally transported and deposited at the cell apex. Meanwhile, active retrograde endocytosis counter balances the exocytosis at the tip which is believed to recycle the excessive exocytic components for multiple rounds of secretion. Therefore, apical exocytosis and endocytosis are the frontline cellular processes which drive the polar growth of pollen tubes, although they represent opposite vesicular trafficking events with distinct underpinning mechanisms. Nevertheless, the molecular basis governing the spatiotemporal crosstalk and counterbalance of exocytosis and endocytosis during pollen tube polarization and growth remains elusive. Here we discuss recent insight into exocytosis and endocytosis in sculpturing high rates of polarized pollen tube growth. In addition, we especially introduce the novel integration of mathematical modeling in uncovering the mysteries of cell polarity and polar cell growth.
PubMed: 33123182
DOI: 10.3389/fpls.2020.572848 -
The New Phytologist Jan 2018Occam's Razor suggests a new model of pollen tube tip growth based on a novel Hechtian oscillator that integrates a periplasmic arabinogalactan glycoprotein-calcium... (Review)
Review
Occam's Razor suggests a new model of pollen tube tip growth based on a novel Hechtian oscillator that integrates a periplasmic arabinogalactan glycoprotein-calcium (AGP-Ca ) capacitor with tip-localized AGPs as the source of tip-focussed cytosolic Ca oscillations: Hechtian adhesion between the plasma membrane and the cell wall of the growing tip acts as a piconewton force transducer that couples the internal stress of a rapidly growing wall to the plasma membrane. Such Hechtian transduction opens stretch-activated Ca channels and activates H -ATPase proton pump efflux that dissociates periplasmic AGP-Ca resulting in a Ca influx that activates exocytosis of wall precursors. Thus, a highly simplified pectic primary cell wall regulates its own synthesis by a Hechtian growth oscillator that regulates overall tip growth. By analogy with the three cryptic inscriptions of the classical Rosetta Stone, the Hechtian Hypothesis translates classical AGP function as a Ca capacitor, pollen tube guide and wall plasticizer into a simple but widely applicable model of tip growth. Even wider ramifications of the Hechtian oscillator may implicate AGPs in osmosensing or gravisensing and other tropisms, leading us yet further towards the Holy Grail of plant growth.
Topics: Cell Membrane; Galactans; Glycoproteins; Mechanotransduction, Cellular; Models, Biological; Pollen Tube
PubMed: 28990197
DOI: 10.1111/nph.14845 -
Plant Signaling & Behavior Sep 2016In order to provide more insight into the function of aquaporins during pollination, we characterized NIP4;1 and NIP4;2, 2 pollen-specific aquaporins of Arabidopsis...
In order to provide more insight into the function of aquaporins during pollination, we characterized NIP4;1 and NIP4;2, 2 pollen-specific aquaporins of Arabidopsis thaliana. NIP4;1 and NIP4;2 displayed high amino acid identity. RT-PCR and GUS promoter analysis showed that they have different expression patterns. NIP4;1 is expressed at low levels in mature pollen, while NIP4;2 is highly expressed only during pollen tube growth. Single T-DNA nip4;1 and nip4;2 mutants and double amiRNA nip4;1 nip4;2 knockdowns showed reduced male fertility due to deficient pollen germination and pollen tube length. Functional assays in oocytes showed that NIP4;1 and NIP4;2 transport water and nonionic solutes. Here, the participation of the different pollen aquaporins in pollen hydration and pollen tube growth is discussed.
Topics: Aquaporins; Arabidopsis; Arabidopsis Proteins; Pollen Tube; Pollination; Promoter Regions, Genetic
PubMed: 27598621
DOI: 10.1080/15592324.2016.1217375 -
Frontiers in Plant Science 2022Successful fertilization of a flowering plant requires tightly controlled cell-to-cell communication between the male pollen grain and the female pistil. Throughout... (Review)
Review
Successful fertilization of a flowering plant requires tightly controlled cell-to-cell communication between the male pollen grain and the female pistil. Throughout pollen-pistil interactions, ligand-receptor kinase signaling is utilized to mediate various checkpoints to promote compatible interactions. In , the later stages of pollen tube growth, ovular guidance and reception in the pistil have been intensively studied, and thus the receptor kinases and the respective ligands in these stages are quite well understood. However, the components of the earlier stages, responsible for recognizing compatible pollen grains and pollen tubes in the upper reproductive tract are less clear. Recently, predicted receptor kinases have been implicated in the initial stages of regulating pollen hydration and supporting pollen tube growth through the upper regions of the reproductive tract in the pistil. The discovery of these additional signaling proteins at the earlier stages of pollen-pistil interactions has further elucidated the mechanisms that employs to support compatible pollen. Despite these advances, many questions remain regarding their specific functions. Here, we review the roles of the different receptor kinases, integrate their proposed functions into a model covering all stages of pollen-pistil interactions, and discuss what remains elusive with regard to their functions, respective binding partners and signaling pathways.
PubMed: 36186080
DOI: 10.3389/fpls.2022.1022684 -
Trends in Plant Science Mar 2024Plant reproduction is a complex, highly-coordinated process in which a single, male germ cell grows through the maternal reproductive tissues to reach and fertilise the... (Review)
Review
Plant reproduction is a complex, highly-coordinated process in which a single, male germ cell grows through the maternal reproductive tissues to reach and fertilise the egg cell. Focussing on Arabidopsis thaliana, we review signalling between male and female partners which is important throughout the pollen tube journey, especially during pollen tube reception at the ovule. Numerous receptor kinases and their coreceptors are implicated in signal perception in both the pollen tube and synergid cells at the ovule entrance, and several specific peptide and carbohydrate ligands for these receptors have recently been identified. Clarifying the interplay between these signals and the downstream responses they instigate presents a challenge for future research and may help to illuminate broader principles of plant cell-cell communication.
Topics: Pollen Tube; Signal Transduction; Arabidopsis; Arabidopsis Proteins; Fertilization
PubMed: 37640641
DOI: 10.1016/j.tplants.2023.07.011 -
Molecular Plant Apr 2015Many recent studies have indicated that cellular communications during plant reproduction, fungal invasion, and defense involve identical or similar molecular players... (Review)
Review
Many recent studies have indicated that cellular communications during plant reproduction, fungal invasion, and defense involve identical or similar molecular players and mechanisms. Indeed, pollen tube invasion and sperm release shares many common features with infection of plant tissue by fungi and oomycetes, as a tip-growing intruder needs to communicate with the receptive cells to gain access into a cell and tissue. Depending on the compatibility between cells, interactions may result in defense, invasion, growth support, or cell death. Plant cells stimulated by both pollen tubes and fungal hyphae secrete, for example, small cysteine-rich proteins and receptor-like kinases are activated leading to intracellular signaling events such as the production of reactive oxygen species (ROS) and the generation of calcium (Ca(2+)) transients. The ubiquitous and versatile second messenger Ca(2+) thereafter plays a central and crucial role in modulating numerous downstream signaling processes. In stimulated cells, it elicits both fast and slow cellular responses depending on the shape, frequency, amplitude, and duration of the Ca(2+) transients. The various Ca(2+) signatures are transduced into cellular information via a battery of Ca(2+)-binding proteins. In this review, we focus on Ca(2+) signaling and discuss its occurrence during plant reproduction and interactions of plant cells with biotrophic filamentous microbes. The participation of Ca(2+) in ROS signaling pathways is also discussed.
Topics: Calcium; Calcium Signaling; Fungi; Plant Cells; Plants; Pollen Tube; Reproduction
PubMed: 25660409
DOI: 10.1016/j.molp.2015.01.023 -
The Plant Journal : For Cell and... May 2022ADF/cofilin is a central regulator of actin dynamics. We previously demonstrated that two closely related Arabidopsis class IIa ADF isovariants, ADF7 and ADF10, are...
ADF/cofilin is a central regulator of actin dynamics. We previously demonstrated that two closely related Arabidopsis class IIa ADF isovariants, ADF7 and ADF10, are involved in the enhancement of actin turnover in pollen, but whether they have distinct functions remains unknown. Here, we further demonstrate that they exhibit distinct functions in regulating actin turnover both in vitro and in vivo. We found that ADF7 binds to ADP-G-actin with lower affinity, and severs and depolymerizes actin filaments less efficiently in vitro than ADF10. Accordingly, in pollen grains, ADF7 more extensively decorates actin filaments and is less freely distributed in the cytoplasm compared to ADF10. We further demonstrate that ADF7 and ADF10 show distinct intracellular localizations during pollen germination, and they have non-equivalent functions in promoting actin turnover in pollen. We thus propose that cooperation and labor division of ADF7 and ADF10 enable pollen cells to achieve exquisite control of the turnover of different actin structures to meet different cellular needs.
Topics: Actin Cytoskeleton; Actins; Arabidopsis; Arabidopsis Proteins; Pollen; Pollen Tube
PubMed: 35233873
DOI: 10.1111/tpj.15723 -
Frontiers in Plant Science 2020In flowering plants, pollen tubes undergo a journey that starts in the stigma and ends in the ovule with the delivery of the sperm cells to achieve double fertilization.... (Review)
Review
In flowering plants, pollen tubes undergo a journey that starts in the stigma and ends in the ovule with the delivery of the sperm cells to achieve double fertilization. The pollen cell wall plays an essential role to accomplish all the steps required for the successful delivery of the male gametes. This extended path involves female tissue recognition, rapid hydration and germination, polar growth, and a tight regulation of cell wall synthesis and modification, as its properties change not only along the pollen tube but also in response to guidance cues inside the pistil. In this review, we focus on the most recent advances in elucidating the molecular mechanisms involved in the regulation of cell wall synthesis and modification during pollen germination, pollen tube growth, and rupture.
PubMed: 33329663
DOI: 10.3389/fpls.2020.599247 -
Plant Molecular Biology Nov 2021Here we review, from a quantitative point of view, the cell biology of protonemal tip growth in the model moss Physcomitrium patens. We focus on the role of the... (Review)
Review
Here we review, from a quantitative point of view, the cell biology of protonemal tip growth in the model moss Physcomitrium patens. We focus on the role of the cytoskeleton, vesicle trafficking, and cell wall mechanics, including reviewing some of the existing mathematical models of tip growth. We provide a primer for existing cell biological tools that can be applied to the future study of tip growth in moss. Polarized cell growth is a ubiquitous process throughout the plant kingdom in which the cell elongates in a self-similar manner. This process is important for nutrient uptake by root hairs, fertilization by pollen, and gametophyte development by the protonemata of bryophytes and ferns. In this review, we will focus on the tip growth of moss cells, emphasizing the role of cytoskeletal organization, cytoplasmic zonation, vesicle trafficking, cell wall composition, and dynamics. We compare some of the existing knowledge on tip growth in protonemata against what is known in pollen tubes and root hairs, which are better-studied tip growing cells. To fully understand how plant cells grow requires that we deepen our knowledge in a variety of forms of plant cell growth. We focus this review on the model plant Physcomitrium patens, which uses tip growth as the dominant form of growth at its protonemal stage. Because mosses and vascular plants shared a common ancestor more than 450 million years ago, we anticipate that both similarities and differences between tip growing plant cells will provide mechanistic information of tip growth as well as of plant cell growth in general. Towards this mechanistic understanding, we will also review some of the existing mathematical models of plant tip growth and their applicability to investigate protonemal morphogenesis. We attempt to integrate the conclusions and data across cell biology and physical modeling to our current state of knowledge of polarized cell growth in P. patens and highlight future directions in the field.
Topics: Actin Cytoskeleton; Algorithms; Bryophyta; Meristem; Models, Biological; Myosins; Plant Cells; Plant Proteins; Plant Roots; Pollen Tube
PubMed: 33825083
DOI: 10.1007/s11103-021-01147-7 -
Frontiers in Plant Science 2020In higher-plant reproduction, the compatibility of pollen tube germination in the pistil is essential for successful double fertilization. It has been reported that ()...
In higher-plant reproduction, the compatibility of pollen tube germination in the pistil is essential for successful double fertilization. It has been reported that () family gene (), expressing in synergid cells, can correctly guide pollen tubes. However, the molecular mechanism underlying the interacting partners to MLOs in the fertilization is still unknown. In our study, we identified the direct protein interaction between CML9 and MLO10 within a non-canonical CaMBD. In GUS reporter assays, expresses in a high level in pollens, whereas can be specifically detected in stigma which reaches up to a peaking level before fertilization. Therefore, the spatio-temporal expression patterns of and are required for the time-window of pollination. When we observed the pollen germination , two mutant alleles dramatically reduced germination rate by 15% compared to wild-type. Consistently, the elongation rate of pollen tubes was obviously slow while manually pollinating pollens to stigmas. Additionally, double mutant alleles had relatively lower rate of seed setting. Taken together, protein interaction between MLO10 and CML9 is supposed to affect pollen tube elongation and further affect seed development.
PubMed: 32793269
DOI: 10.3389/fpls.2020.01119