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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 -
Proceedings of the National Academy of... Nov 2018Plant reproduction requires long-distance growth of a pollen tube to fertilize the female gametophyte. Prior reports suggested that mutations altering synthesis of...
Plant reproduction requires long-distance growth of a pollen tube to fertilize the female gametophyte. Prior reports suggested that mutations altering synthesis of flavonoids, plant specialized metabolites that include flavonols and anthocyanins, impair pollen development in several species, but the mechanism by which flavonols enhanced fertility was not defined. Here, we used genetic approaches to demonstrate that flavonols enhanced pollen development by reducing the abundance of reactive oxygen species (ROS). We further showed that flavonols reduced high-temperature stress-induced ROS accumulation and inhibition of pollen tube growth. The () tomato mutant had reduced flavonol accumulation in pollen grains and tubes. This mutant produced fewer pollen grains and had impaired pollen viability, germination, tube growth, and tube integrity, resulting in reduced seed set. Consistent with flavonols acting as ROS scavengers, had elevated levels of ROS. The pollen viability, tube growth and integrity defects, and ROS accumulation in were reversed by genetic complementation. Inhibition of ROS synthesis or scavenging of excess ROS with an exogenous antioxidant treatment also reversed the phenotypes, indicating that flavonols function by reducing ROS levels. Heat stress resulted in increased ROS in pollen tubes and inhibited tube growth, with more pronounced effects in the mutant that could be rescued by antioxidant treatment. These results are consistent with increased ROS inhibiting pollen tube growth and with flavonols preventing ROS from reaching damaging levels. These results reveal that flavonol metabolites regulate plant sexual reproduction at both normal and elevated temperatures by maintaining ROS homeostasis.
Topics: Anthocyanins; Flavonols; Heat-Shock Response; Hot Temperature; Solanum lycopersicum; Pollen; Pollen Tube; Pollination; Reactive Oxygen Species; Seeds; Stress, Physiological
PubMed: 30413622
DOI: 10.1073/pnas.1811492115 -
Plant Reproduction Mar 2021Analyses of secretomes of in vitro grown pollen tubes from Amborella, maize and tobacco identified many components of processes associated with the cell wall, signaling...
Analyses of secretomes of in vitro grown pollen tubes from Amborella, maize and tobacco identified many components of processes associated with the cell wall, signaling and metabolism as well as novel small secreted peptides. Flowering plants (angiosperms) generate pollen grains that germinate on the stigma and produce tubes to transport their sperm cells cargo deep into the maternal reproductive tissues toward the ovules for a double fertilization process. During their journey, pollen tubes secrete many proteins (secreted proteome or secretome) required, for example, for communication with the maternal reproductive tissues, to build a solid own cell wall that withstands their high turgor pressure while softening simultaneously maternal cell wall tissue. The composition and species specificity or family specificity of the pollen tube secretome is poorly understood. Here, we provide a suitable method to obtain the pollen tube secretome from in vitro grown pollen tubes of the basal angiosperm Amborella trichopoda (Amborella) and the Poaceae model maize. The previously published secretome of tobacco pollen tubes was used as an example of eudicotyledonous plants in this comparative study. The secretome of the three species is each strongly different compared to the respective protein composition of pollen grains and tubes. In Amborella and maize, about 40% proteins are secreted by the conventional "classic" pathway and 30% by unconventional pathways. The latter pathway is expanded in tobacco. Proteins enriched in the secretome are especially involved in functions associated with the cell wall, cell surface, energy and lipid metabolism, proteolysis and redox processes. Expansins, pectin methylesterase inhibitors and RALFs are enriched in maize, while tobacco secretes many proteins involved, for example, in proteolysis and signaling. While the majority of proteins detected in the secretome occur also in pollen grains and pollen tubes, and correlate in the number of mapped peptides with relative gene expression levels, some novel secreted small proteins were identified. Moreover, the identification of secreted proteins containing pro-peptides indicates that these are processed in the apoplast. In conclusion, we provide a proteome resource from three distinct angiosperm clades that can be utilized among others to study the localization, abundance and processing of known secreted proteins and help to identify novel pollen tube secreted proteins for functional studies.
Topics: Magnoliopsida; Ovule; Peptides; Pollen Tube; Nicotiana; Zea mays
PubMed: 33258014
DOI: 10.1007/s00497-020-00399-5 -
Massively Parallelized Pollen Tube Guidance and Mechanical Measurements on a Lab-on-a-Chip Platform.PloS One 2016Pollen tubes are used as a model in the study of plant morphogenesis, cellular differentiation, cell wall biochemistry, biomechanics, and intra- and intercellular...
Pollen tubes are used as a model in the study of plant morphogenesis, cellular differentiation, cell wall biochemistry, biomechanics, and intra- and intercellular signaling. For a "systems-understanding" of the bio-chemo-mechanics of tip-polarized growth in pollen tubes, the need for a versatile, experimental assay platform for quantitative data collection and analysis is critical. We introduce a Lab-on-a-Chip (LoC) concept for high-throughput pollen germination and pollen tube guidance for parallelized optical and mechanical measurements. The LoC localizes a large number of growing pollen tubes on a single plane of focus with unidirectional tip-growth, enabling high-resolution quantitative microscopy. This species-independent LoC platform can be integrated with micro-/nano-indentation systems, such as the cellular force microscope (CFM) or the atomic force microscope (AFM), allowing for rapid measurements of cell wall stiffness of growing tubes. As a demonstrative example, we show the growth and directional guidance of hundreds of lily (Lilium longiflorum) and Arabidopsis (Arabidopsis thaliana) pollen tubes on a single LoC microscopy slide. Combining the LoC with the CFM, we characterized the cell wall stiffness of lily pollen tubes. Using the stiffness statistics and finite-element-method (FEM)-based approaches, we computed an effective range of the linear elastic moduli of the cell wall spanning the variability space of physiological parameters including internal turgor, cell wall thickness, and tube diameter. We propose the LoC device as a versatile and high-throughput phenomics platform for plant reproductive and development biology using the pollen tube as a model.
Topics: Cell Wall; Elastic Modulus; Lab-On-A-Chip Devices; Lilium; Pollen Tube; Pollination
PubMed: 27977748
DOI: 10.1371/journal.pone.0168138 -
Science China. Life Sciences Sep 2019
Review
Topics: Cysteine; Fertility; Gene Expression Regulation, Plant; Mutation; Peptides; Pollen Tube; Pollination; Protein Serine-Threonine Kinases; Species Specificity
PubMed: 31444684
DOI: 10.1007/s11427-019-9819-3 -
The New Phytologist Nov 2019The causative link between phenotypic divergence and reproductive isolation is an important but poorly understood part of ecological speciation. We studied the effects...
The causative link between phenotypic divergence and reproductive isolation is an important but poorly understood part of ecological speciation. We studied the effects of floral-tube length variation on pollen placement/receipt positions and reproductive isolation. In a population of Lapeirousia anceps (Iridaceae) with bimodal floral-tube lengths, we labelled pollen of short- and long-tubed flowers with different colour fluorescent nanoparticles (quantum dots). This enabled us to map pollen placement by long- and short-tubed flowers on the only floral visitor, a long-proboscid fly. Furthermore, it allowed us to quantify pollen movement within and between short- and long-tubed flowers. Short- and long-tubed flowers placed pollen on different parts of the pollinator, and long-tubed flowers placed more pollen per visit than short-tubed flowers. This resulted in assortative pollen receipt (most pollen received comes from the same phenotype) and strong but asymmetric reproductive isolation, where short-tubed plants are more reproductively isolated than long-tubed plants. These results suggest that floral-tube length divergence can promote mechanical isolation in plants through divergence in pollen placement sites on pollinators. Consequently, in concert with other reproductive isolation mechanisms, selection for differences in floral-tube length can play an important role in ecological speciation of plants.
Topics: Animals; Biodiversity; Diptera; Iridaceae; Movement; Pollen Tube; Pollination; Reproductive Isolation; Species Specificity
PubMed: 31148172
DOI: 10.1111/nph.15971 -
Bio Systems Nov 2018One of the most challenging questions in cell and developmental biology is how molecular signals are translated into mechanical forces that ultimately drive cell growth...
One of the most challenging questions in cell and developmental biology is how molecular signals are translated into mechanical forces that ultimately drive cell growth and motility. Despite an impressive body of literature demonstrating the importance of cytoskeletal and motor proteins as well as osmotic stresses for cell developmental mechanics, a host of dissenting evidence strongly suggests that these factors per se cannot explain growth mechanics even at the level of a single tip-growing cell. The present study addresses this issue by exploring fundamental interrelations between electrical and mechanical fields operating in cells. In the first instance, we employ a simplified but instructive model of a quiescent cell to demonstrate that even in a quasi-equilibrium state, ion transport processes are conditioned principally by mechanical tenets. Then we inquire into the electromechanical conjugacy in growing pollen tubes as biologically relevant and physically tractable developmental systems owing to their extensively characterized growth-associated ionic fluxes and strikingly polarized growth and morphology. A comprehensive analysis of the multifold stress pattern in the growing apices of pollen tubes suggests that tip-focused ionic fluxes passing through the polyelectrolyte-rich apical cytoplasm give rise to electrokinetic flows that actualize otherwise isotropic intracellular turgor into anisotropic stress field. The stress anisotropy can be then imparted from the apical cytoplasm to the abutting frontal cell wall to induce its local extension and directional cell growth. Converging lines of evidence explored in the concluding sections attest that tip-focused ionic fluxes and associated interfacial transport phenomena are not specific for pollen tubes but are also employed by a vast variety of algal, plant, fungal and animal cells, rendering their cytoplasmic stress fields essentially anisotropic and ultimately instrumental in cell shaping, growth and motility.
Topics: Animals; Cell Cycle; Cell Proliferation; Cell Shape; Cell Wall; Cytoplasm; Cytoskeleton; Ions; Kinetics; Morphogenesis; Osmosis; Osmotic Pressure; Pollen Tube; Pollination; Stress, Mechanical
PubMed: 30300677
DOI: 10.1016/j.biosystems.2018.10.004 -
Nature Mar 2016Directional control of tip-growing cells is essential for proper tissue organization and cell-to-cell communication in animals and plants. In the sexual reproduction of...
Directional control of tip-growing cells is essential for proper tissue organization and cell-to-cell communication in animals and plants. In the sexual reproduction of flowering plants, the tip growth of the male gametophyte, the pollen tube, is precisely guided by female cues to achieve fertilization. Several female-secreted peptides have recently been identified as species-specific attractants that directly control the direction of pollen tube growth. However, the method by which pollen tubes precisely and promptly respond to the guidance signal from their own species is unknown. Here we show that tip-localized pollen-specific receptor-like kinase 6 (PRK6) with an extracellular leucine-rich repeat domain is an essential receptor for sensing of the LURE1 attractant peptide in Arabidopsis thaliana under semi-in-vivo conditions, and is important for ovule targeting in the pistil. PRK6 interacted with pollen-expressed ROPGEFs (Rho of plant guanine nucleotide-exchange factors), which are important for pollen tube growth through activation of the signalling switch Rho GTPase ROP1 (refs 7, 8). PRK6 conferred responsiveness to AtLURE1 in pollen tubes of the related species Capsella rubella. Furthermore, our genetic and physiological data suggest that PRK6 signalling through ROPGEFs and sensing of AtLURE1 are achieved in cooperation with the other PRK family receptors, PRK1, PRK3 and PRK8. Notably, the tip-focused PRK6 accumulated asymmetrically towards an external AtLURE1 source before reorientation of pollen tube tip growth. These results demonstrate that PRK6 acts as a key membrane receptor for external AtLURE1 attractants, and recruits the core tip-growth machinery, including ROP signalling proteins. This work provides insights into the orchestration of efficient pollen tube growth and species-specific pollen tube attraction by multiple receptors during male-female communication.
Topics: Arabidopsis; Arabidopsis Proteins; Capsella; GTP-Binding Proteins; Mutation; Ovule; Phenotype; Phosphotransferases; Pollen Tube; Protein Serine-Threonine Kinases; Protein Structure, Tertiary; Receptors, Cell Surface; Reproduction; Signal Transduction; Species Specificity
PubMed: 26961657
DOI: 10.1038/nature17413 -
Protoplasma Nov 2021The shape of the apical region of lily pollen tube changes rhythmically as the growth rate of the tube oscillates becoming alternately more prolate then back to oblate....
The shape of the apical region of lily pollen tube changes rhythmically as the growth rate of the tube oscillates becoming alternately more prolate then back to oblate. We quantified shape change by calculating the curvature of the cross-sectional edge of the pollen tube tip and cross-correlating curvature changes with growth rate. The apical region takes the form of a partial elliptical spheroid, with variation in the length and location of the minor axis. During oscillation curvature profiles show a sharp increase in curvature at the "shoulders" of the apex when oblate, 4-7 μm from the flatter central zone. As the tip becomes more prolate, the "shoulders" decrease rapidly in curvature and move towards the growth axis as curvature at the tip increases. We understand curvature changes to represent differential changes in local wall expansion rates, driven by uniform turgor pressure and mediated by changes in wall polysaccharides. To become more oblate, the tip region must become less extensible than the "shoulder" region. And, as the tip becomes more prolate, the increased curvature must be due to increased local expansion. We found that changes in the growth velocity of the "shoulders" of the cell measured as the progress of the cell edge along the growth axis are cyclically out of phase with growth velocity at the tip such that the shoulder regions lag for part of the oscillation cycle, then "catch up" as the growth rate at the tip reaches a maximum and begins to decline. In this way the cell becomes oblate. Cell shape and growth rate oscillate in concert and are functionally related. Spatial change in edge growth rate points to important cellular locations for further investigation of vesicle movement and exocytosis, calcium gradients, and actin dynamics in lily pollen tubes.
Topics: Cell Wall; Cross-Sectional Studies; Exocytosis; Lilium; Pollen Tube
PubMed: 34414478
DOI: 10.1007/s00709-021-01694-2 -
Plant Physiology Jan 2017Pollen-pistil interactions contribute to mate selection at the postmating, prezygotic level. (Review)
Review
Pollen-pistil interactions contribute to mate selection at the postmating, prezygotic level.
Topics: Flowers; Magnoliopsida; Papaver; Pollen; Pollen Tube; Pollination; Reproduction; Self-Incompatibility in Flowering Plants; Species Specificity
PubMed: 27899537
DOI: 10.1104/pp.16.01286