scholarly journals Exocytosis and endocytosis: coordinating and fine-tuning the polar tip growth domain in pollen tubes

2020 ◽  
Vol 71 (8) ◽  
pp. 2428-2438 ◽  
Author(s):  
Jingzhe Guo ◽  
Zhenbiao Yang
Keyword(s):  
Cell Wall ◽  
Rho Gtpases ◽  
Intracellular Signaling ◽  
Tip Growth ◽  
Apical Cell ◽  
Turgor Pressure ◽  
Pollen Tubes ◽  
Fine Tuning ◽  
Rop Gtpase ◽  
Specialized Form

Abstract Pollen tubes rapidly elongate, penetrate, and navigate through multiple female tissues to reach ovules for sperm delivery by utilizing a specialized form of polar growth known as tip growth. This process requires a battery of cellular activities differentially occurring at the apical growing region of the plasma membrane (PM), such as the differential cellular signaling involving calcium (Ca2+), phospholipids, and ROP-type Rho GTPases, fluctuation of ions and pH, exocytosis and endocytosis, and cell wall construction and remodeling. There is an emerging understanding of how at least some of these activities are coordinated and/or interconnected. The apical active ROP modulates exocytosis to the cell apex for PM and cell wall expansion differentially occurring at the tip. The differentiation of the cell wall involves at least the preferential distribution of deformable pectin polymers to the apex and non-deformable pectin polymers to the shank of pollen tubes, facilitating the apical cell expansion driven by high internal turgor pressure. Recent studies have generated inroads into how the ROP GTPase-based intracellular signaling is coordinated spatiotemporally with the external wall mechanics to maintain the tubular cell shape and how the apical cell wall mechanics are regulated to allow rapid tip growth while maintaining the cell wall integrity under the turgor pressure. Evidence suggests that exocytosis and endocytosis play crucial but distinct roles in this spatiotemporal coordination. In this review, we summarize recent advances in the regulation and coordination of the differential pectin distribution and the apical domain of active ROP by exocytosis and endocytosis in pollen tubes.

Integration and regulation of hyphal tip growth

1995 ◽  
Vol 73 (S1) ◽  
pp. 131-139 ◽  
Author(s):  
I. Brent Heath
Keyword(s):  
Cell Wall ◽  
Tip Growth ◽  
Apical Cell ◽  
Turgor Pressure ◽  
Feedback Regulation ◽  
Regulation Mechanism ◽  
Hyphal Tip Growth ◽  
Species Specific ◽  
Stretch Activated Channels ◽  
Hyphal Tip

Hyphal tip growth is an exquisitely controlled process that forms developmentally regulated, species-specific, even-diameter tubes at rates of up to about 50 μm/min. The traditional view is that this process results from the balance between the expansive force of turgor pressure and the controlled extensibility of the apical cell wall. While these elements are involved, the model places regulation into either the global domain (turgor pressure) or the extracellular environment (the cell wall), neither of which seem well suited to the level of control evinced. Recent evidence suggests that F-actin-rich elements of the cytoskeleton are important in tip morphogenesis. Our current models propose that tip expansion is regulated (restrained under normal turgor pressure and protruded under low turgor) by a peripheral network of F-actin that is attached to the plasmalemma and the cell wall by integrin-containing linkages, thus placing control in the cytoplasm where it is accessible to normal intracellular regulatory systems. The F-actin system also functions in cytoplasmic and organelle motility; control of plasmalemma-located, stretch-activated, Ca2+-transporting, ion channel distribution; vectoral vesicle transport; and exocytosis. Regulation of the system may involve Ca2+, the concentration of which is influenced by the tip-high gradient of the stretch-activated channels, thus suggesting a possible feedback regulation mechanism. Key words: tip growth, fungi, stretch-activated channels, F-actin, Ca2+, hyphae.

Pronounced cytoplasmic pH gradients are not required for tip growth in plant and fungal cells

1997 ◽  
Vol 110 (10) ◽  
pp. 1187-1198 ◽  
Author(s):  
R.M. Parton ◽  
S. Fischer ◽  
R. Malho ◽  
O. Papasouliotis ◽  
T.C. Jelitto ◽  
...  
Keyword(s):  
Tip Growth ◽  
Cell Types ◽  
Pollen Tubes ◽  
Fine Tuning ◽  
Cytoplasmic Ph ◽  
Dual Emission ◽  
Ph Gradients ◽  
Longitudinal Gradients ◽  
External Ph

The existence of pronounced cytoplasmic pH gradients within the apices of tip-growing cells, and the role of cytoplasmic pH in regulating tip growth, were investigated in three different cell types: vegetative hyphae of Neurospora crassa; pollen tubes of Agapanthus umbellatus; and rhizoids of Dryopteris affinis gametophytes. Examination of cytoplasmic pH in growing cells was performed by simultaneous, dual emission confocal ratio imaging of the pH-sensitive probe carboxy SNARF-1. Considerable attention was paid to the fine tuning of dye loading and imaging parameters to minimise cellular perturbation and assess the extent of dye partitioning into organelles. With optimal conditions, cytoplasmic pH was measured routinely with a precision of between +/−0.03 and +/−0.06 of a pH unit and a spatial resolution of 2.3 microm2. Based on in vitro calibration, estimated values of mean cytoplasmic pH for cells loaded with dye-ester were between 7.15 and 7.25 for the three cell types. After pressure injecting Neurospora hyphae with dextran-conjugated dye, however, the mean cytoplasmic pH was estimated to be 7.57. Dextran dyes are believed to give a better estimate of cytoplasmic pH because of their superior localisation and retention within the cytosol. No significant cytoplasmic pH gradient (delta pH of >0.1 unit) was observed within the apical 50 microm in growing cells of any of the three cell types. Acidification or alkalinisation of the cytoplasm in Neurospora hyphae, using a cell permeant weak acid (propionic acid at pH 7.0) or weak base (trimethylamine at pH 8.0), slowed down but did not abolish growth. However, similar manipulation of the cytoplasmic pH of Agapanthus pollen tubes and Dryopteris rhizoids completely inhibited growth. Modification of external pH affected the growth pattern of all cell types. In hyphae and pollen tubes, changes in external pH were found to have a small transient effect on cytoplasmic pH but the cells rapidly readjusted towards their original pH. Our results suggest that pronounced longitudinal gradients in cytoplasmic pH are not essential for the regulation of tip growth.

Fountain streaming contributes to fast tip-growth through regulating the gradients of turgor pressure and concentration in pollen tubes

Soft Matter ◽  
2017 ◽  
Vol 13 (16) ◽  
pp. 2919-2927 ◽  
Author(s):  
ShaoBao Liu ◽  
Han Liu ◽  
ShangSheng Feng ◽  
Min Lin ◽  
Feng Xu ◽  
...  
Keyword(s):  
Tip Growth ◽  
Turgor Pressure ◽  
Pollen Tubes ◽  
Fountain Streaming

scholarly journals Comparative analyses of angiosperm secretomes identify apoplastic pollen tube functions and novel secreted peptides

2020 ◽  
Author(s):  
María Flores-Tornero ◽  
Lele Wang ◽  
David Potěšil ◽  
Said Hafidh ◽  
Frank Vogler ◽  
...  
Keyword(s):  
Cell Wall ◽  
Pollen Tube ◽  
Turgor Pressure ◽  
Pollen Grains ◽  
Pollen Tubes ◽  
Secreted Proteins ◽  
Reproductive Tissues ◽  
Small Proteins ◽  
Secreted Peptides

Abstract Key message 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. Abstract 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.

scholarly journals Vav1 and Ly-GDI Two Regulators of Rho GTPases, Function Cooperatively as Signal Transducers in T Cell Antigen Receptor-induced Pathways

2002 ◽  
Vol 277 (51) ◽  
pp. 50121-50130 ◽  
Author(s):  
Maya Groysman ◽  
Idit Hornstein ◽  
Andres Alcover ◽  
Shulamit Katzav
Keyword(s):  
T Cells ◽  
T Cell ◽  
Rho Gtpases ◽  
Intracellular Signaling ◽  
Calcium Mobilization ◽  
Hematopoietic Cell ◽  
Fine Tuning ◽  
Guanine Nucleotide ◽  
Nucleotide Exchange ◽  
Activated T Cells

The Rho family GTPases are pivotal for T cell signaling; however, the regulation of these proteins is not fully known. One well studied regulator of Rho GTPases is Vav1; a hematopoietic cell-specific guanine nucleotide exchange factor critical for signaling in T cells, including stimulation of the nuclear factor of activated T cells (NFAT). Surprisingly, Vav1 associates with Ly-GDI, a hematopoietic cell-specific guanine nucleotide dissociation inhibitor of Rac. Here, we studied the functional significance of the interaction between Vav1 and Ly-GDI in T cells. Upon organization of the immunological synapse, both Ly-GDI and Vav1 relocalize to T cell extensions in contact with the antigen-presenting cell. Ly-GDI is phosphorylated on tyrosine residues following T cell receptor stimulation, and it associates with the Src homology 2 region of an adapter protein, Shc. In addition, the interaction between Ly-GDI and Vav1 requires tyrosine phosphorylation. Overexpression of Ly-GDI alone is inhibitory to NFAT stimulation and calcium mobilization. However, when co-expressed with Vav1, Ly-GDI enhances Vav1 induction of NFAT activation, phospholipase Cγ phosphorylation, and calcium mobilization. Moreover, Ly-GDI does not alter the regulation of these phenomena when coexpressed with oncogenic Vav1. Since oncogenic Vav1 does not bind Ly-GDI, this suggests that the functional cooperativity of Ly-GDI and Vav1 is dependent upon their association. Thus, our data suggest that the interaction of Vav1 and Ly-GDI creates a fine tuning mechanism for the regulation of intracellular signaling pathways leading to NFAT stimulation.

scholarly journals Oscillatory ROP GTPase Activation Leads the Oscillatory Polarized Growth of Pollen Tubes

2005 ◽  
Vol 16 (11) ◽  
pp. 5385-5399 ◽  
Author(s):  
Jae-Ung Hwang ◽  
Ying Gu ◽  
Yong-Jik Lee ◽  
Zhenbiao Yang
Keyword(s):  
Gene Expression ◽  
Molecular Mechanisms ◽  
Tip Growth ◽  
Rho Gtpase ◽  
Cell Movement ◽  
Pollen Tubes ◽  
Common Mechanism ◽  
Rop Gtpase ◽  
Growth Oscillation ◽  
Gtpase Activation

Oscillation regulates a wide variety of processes ranging from chemotaxis in Dictyostelium through segmentation in vertebrate development to circadian rhythms. Most studies on the molecular mechanisms underlying oscillation have focused on processes requiring a rhythmic change in gene expression, which usually exhibit a periodicity of >10 min. Mechanisms that control oscillation with shorter periods (<10 min), presumably independent of gene expression changes, are poorly understood. Oscillatory pollen tube tip growth provides an excellent model to investigate such mechanisms. It is well established that ROP1, a Rho-like GTPase from plants, plays an essential role in polarized tip growth in pollen tubes. In this article, we demonstrate that tip-localized ROP1 GTPase activity oscillates in the same frequency with growth oscillation, and leads growth both spatially and temporally. Tip growth requires the coordinate action of two ROP1 downstream pathways that promote the accumulation of tip-localized Ca2+and actin microfilaments (F-actin), respectively. We show that the ROP1 activity oscillates in a similar phase with the apical F-actin but apparently ahead of tip-localized Ca2+. Furthermore, our observations support the hypothesis that the oscillation of tip-localized ROP activity and ROP-dependent tip growth in pollen tubes is modulated by the two temporally coordinated downstream pathways, an early F-actin assembly pathway and a delayed Ca2+gradient-forming pathway. To our knowledge, our report is the first to demonstrate the oscillation of Rho GTPase signaling, which may be a common mechanism underlying the oscillation of actin-dependent processes such as polar growth, cell movement, and chemotaxis.

Defective control of growth rate and cell diameter in tip-growing root hairs of the rhd4 mutant of Arabidopsis thaliana

1999 ◽  
Vol 77 (4) ◽  
pp. 494-507 ◽  
Author(s):  
M E Galway ◽  
D C Lane ◽  
J W Schiefelbein
Keyword(s):  
Growth Rate ◽  
Arabidopsis Thaliana ◽  
Cell Wall ◽  
Osmotic Stress ◽  
Tip Growth ◽  
Turgor Pressure ◽  
Root Hairs ◽  
Recessive Mutation ◽  
Cell Diameter ◽  
Hair Diameter

A recessive mutation in the RHD4 gene of Arabidopsis thaliana L. affects the control of tip growth in seedling root hairs. Fully grown rhd4 root hairs are half the length of wild-type (WT) hairs. The hairs are wider, and they vary in diameter during tip growth. Light microscopy and motion analysis revealed that rhd4 hairs grow more slowly and that hair growth rate varies more than in WT hairs. Hair diameter increases at the rhd4 hair tips when tip growth slows. Ultrastructural analysis revealed cell wall thickenings in some mutant hairs. WT hairs were grown in a hyperosmotic medium in an attempt to mimic the rhd4 hairs and investigate the control of root hair morphology. Osmotic stress increased WT hair diameter and induced hair bulging and also increased the diameters of rhd4 hairs. Osmotic stress could disrupt tip growth through reduced turgor pressure and (or) reduced concentrations of cytosolic calcium. Together these results indicate that RHD4 is required to maintain a uniform rate of tip growth in root hairs.Key words: Arabidopsis thaliana, cell wall, cryofixation, mutant, root hairs, tip growth.

scholarly journals An Evolutionarily Conserved Receptor-like Kinases Signaling Module Controls Cell Wall Integrity During Tip-Growth

2019 ◽  
Author(s):  
Jens Westermann ◽  
Susanna Streubel ◽  
Christina Maria Franck ◽  
Roswitha Lentz ◽  
Liam Dolan ◽  
...  
Keyword(s):  
Cell Wall ◽  
Tip Growth ◽  
Root Hairs ◽  
Pollen Tubes ◽  
Cell Wall Integrity ◽  
Marchantia Polymorpha ◽  
Evolutionarily Conserved ◽  
Receptor Kinases ◽  
The Common ◽  
Encoding Genes

AbstractRooting cells and pollen tubes – key adaptative innovations that evolved during the colonization and subsequent radiation of plants on land – expand by tip-growth. Tip-growth relies on a tight coordination between the protoplast growth and the synthesis/remodeling of the external cell wall. In root hairs and pollen tubes of the seed plant Arabidopsis thaliana, cell wall integrity (CWI) mechanisms monitor this coordination through the Malectin-like receptor kinases (MLRs) such as AtANXUR1 and AtFERONIA that act upstream of the AtMARIS PTI1-like kinase. Here, we show that rhizoid growth in the early diverging plant, Marchantia polymorpha, is also controlled by an MLR and PTI1-like signaling module. Rhizoids, root hairs and pollen tubes respond similarly to disruption of MLR and PTI1-like encoding genes. Thus, the MLR/PTI1-like signaling module that controls CWI during tip-growth is conserved between M. polymorpha and A. thaliana suggesting it was active in the common ancestor of land plants.

scholarly journals An image analysis method to survey the dynamics of polar protein abundance in the regulation of tip growth

2020 ◽  
Vol 133 (22) ◽  
pp. jcs252064 ◽  
Author(s):  
Sarah Taheraly ◽  
Dmitry Ershov ◽  
Serge Dmitrieff ◽  
Nicolas Minc
Keyword(s):  
Cell Wall ◽  
Image Analysis ◽  
Rho Gtpases ◽  
Tip Growth ◽  
Control Cell ◽  
Large Data ◽  
Life Cycles ◽  
Growth Speed ◽  
Protein Abundance ◽  
Canonical Surface

ABSTRACTTip growth is critical for the lifestyle of many walled cells. In yeast and fungi, this process is typically associated with the polarized deposition of conserved tip factors, including landmarks, Rho GTPases, cytoskeleton regulators, and membrane and cell wall remodelers. Because tip growth speeds may vary extensively between life cycles or species, we asked whether the local amount of specific polar elements could determine or limit tip growth speeds. Using the model fission yeast, we developed a quantitative image analysis pipeline to dynamically correlate single tip elongation speeds and polar protein abundance in large data sets. We found that polarity landmarks are typically diluted by growth. In contrast, tip growth speed is positively correlated with the local amount of factors related to actin, secretion or cell wall remodeling, but, surprisingly, exhibits long saturation plateaus above certain concentrations of those factors. Similar saturation observed for Spitzenkörper components in much faster growing fungal hyphae suggests that elements independent of canonical surface remodelers may limit single tip growth. This work provides standardized methods and resources to decipher the complex mechanisms that control cell growth.This article has an associated First Person interview with Sarah Taheraly, joint first author of the paper.

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