scholarly journals Mechanical properties of the stigmatic cell wall mediate pollen tube path in Arabidopsis

2018 ◽  
Author(s):  
Lucie Riglet ◽  
Frédérique Rozier ◽  
Chie Kodera ◽  
Isabelle Fobis-Loisy ◽  
Thierry Gaude
Keyword(s):  
Cell Wall ◽  
Pollen Tube ◽  
Cell Shape ◽  
Cell Imaging ◽  
Pollen Tubes ◽  
Mechanical Anisotropy ◽  
Cellulose Microfibrils ◽  
Mechanical Forces ◽  
Cortical Microtubules ◽  
Isotropic Reorientation

ABSTRACTSuccessful fertilization in angiosperms depends on the proper trajectory of pollen tubes through the pistil tissues to reach the ovules. Pollen tubes first grow within the cell wall of the papilla cells, applying pressure to the cell. Mechanical forces are known to play a major role in plant cell shape by controlling the orientation of cortical microtubules (CMTs), which in turn mediate deposition of cellulose microfibrils (CMFs). Here, by combining cell imaging and genetic approaches, we show that isotropic reorientation of CMTs and CMFs in aged and katanin1-5 (ktn1-5) papilla cells is accompanied by a tendency of pollen tubes to coil around the papillae. Furthermore, we uncover that aged and ktn1-5 papilla cells have a softer cell wall and provide less resistance to pollen tube growth. Our results reveal an unexpected role for KTN1 in pollen tube guidance by ensuring mechanical anisotropy of the papilla cell wall.

scholarly journals KATANIN-dependent mechanical properties of the stigmatic cell wall mediate the pollen tube path in Arabidopsis

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Lucie Riglet ◽  
Frédérique Rozier ◽  
Chie Kodera ◽  
Simone Bovio ◽  
Julien Sechet ◽  
...  
Keyword(s):  
Mechanical Properties ◽  
Cell Wall ◽  
Pollen Tube ◽  
Cell Walls ◽  
Cell Shape ◽  
Pollen Tubes ◽  
Mechanical Anisotropy ◽  
Cellulose Microfibrils ◽  
Cortical Microtubules ◽  
Isotropic Reorientation

Successful fertilization in angiosperms depends on the proper trajectory of pollen tubes through the pistil tissues to reach the ovules. Pollen tubes first grow within the cell wall of the papilla cells, applying pressure to the cell. Mechanical forces are known to play a major role in plant cell shape by controlling the orientation of cortical microtubules (CMTs), which in turn mediate deposition of cellulose microfibrils (CMFs). Here, by combining imaging, genetic and chemical approaches, we show that isotropic reorientation of CMTs and CMFs in aged Col-0 and katanin1-5 (ktn1-5) papilla cells is accompanied by a tendency of pollen tubes to coil around the papillae. We show that this coiled phenotype is associated with specific mechanical properties of the cell walls that provide less resistance to pollen tube growth. Our results reveal an unexpected role for KTN1 in pollen tube guidance on the stigma by ensuring mechanical anisotropy of the papilla cell wall.

Alignment of Cortical Microtubules by Anisotropic Wall Stresses

1990 ◽  
Vol 17 (6) ◽  
pp. 601 ◽  
Author(s):  
RE Williamson
Keyword(s):  
Cell Shape ◽  
Feedback Loop ◽  
Plant Cells ◽  
Cellulose Microfibrils ◽  
Specific Information ◽  
Mechanical Forces ◽  
Cortical Microtubules ◽  
Directional Information ◽  
Cell Position ◽  
Single Protein

Anisotropic mechanical forces exist in the walls of all turgid plant cells except those of spherical unicells. These forces potentially offer the cell important directional information regarding its major and minor axes, and the more complicated force patterns expected in multicellular organs could offer location-specific information. A mechanism is proposed to measure directional forces in the wall as deformations (strain) of molecules associated with cellulose microfibrils and transmit the information across the plasma membrane to orient cortical microtubules. Because microtubules in turn orient the synthesis of the cellulose microfibrils that determine the direction of future cell expansion, a feedback loop is established relating future cell shape to present cell shape and cell position. The loop can provide positive feedback to magnify a small asymmetry in shape, to reinforce an existing growth axis in a cylindrical cell or, by modification of the proteins postulated to convey directional information between wall and cytoplasm, the loop can be broken and the same directional information used to establish a new orientation for cortical microtubules. In this way, modification of a single protein replaces a transverse microtubule array with a helical one.

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 The Structure and Plastic Properties of the Cell Wall of Nitella in Relation to Extension Growth

1966 ◽  
Vol 19 (3) ◽  
pp. 439 ◽  
Author(s):  
MC Probine ◽  
NF Barber
Keyword(s):  
Mechanical Properties ◽  
Cell Wall ◽  
Cell Growth ◽  
Elastic Properties ◽  
Cell Shape ◽  
Cellulose Microfibrils ◽  
Theoretical Treatment ◽  
Plastic Properties ◽  
Growing Cell ◽  
Plastic Matrix

The internodal cells of Nitella opaca L. have been used in earlier studies to assess the part which mechanical properties of the wall may play in the control of cell growth (Probine and Preston 1962). The wall is mechanically anisotropic in both its plastic and elastic properties, and it is shown in this paper by an approximate theoretical treatment that a mat of cellulose microfibrils, embedded in a plastic matrix and having a distribution in the plane of the wall like that observed in Nitella, would lead to longitUdinal and transverse plastic extensions in the ratio observed in the growing cell. Factors which would affect cell shape are discussed.

scholarly journals Plant AP180 N-Terminal Homolog Proteins Are Involved in Clathrin-Dependent Endocytosis during Pollen Tube Growth in Arabidopsis thaliana

2019 ◽  
Vol 60 (6) ◽  
pp. 1316-1330 ◽  
Author(s):  
Minako Kaneda ◽  
Chlo� van Oostende-Triplet ◽  
Youssef Chebli ◽  
Christa Testerink ◽  
Sebastian Y Bednarek ◽  
...  
Keyword(s):  
Cell Wall ◽  
Pollen Tube ◽  
Membrane Trafficking ◽  
Pollen Tubes ◽  
Wall Material ◽  
Knockout Mutant ◽  
Cell Wall Assembly ◽  
Morphological Defects ◽  
Fluorescent Tagging

Abstract Polarized cell growth in plants is maintained under the strict control and exquisitely choreographed balance of exocytic and endocytic membrane trafficking. The pollen tube has become a model system for rapid polar growth in which delivery of cell wall material and membrane recycling are controlled by membrane trafficking. Endocytosis plays an important role that is poorly understood. The plant AP180 N-Terminal Homolog (ANTH) proteins are putative homologs of Epsin 1 that recruits clathrin to phosphatidylinositol 4, 5-bisphosphate (PIP2) containing membranes to facilitate vesicle budding during endocytosis. Two Arabidopsis ANTH encoded by the genes AtAP180 and AtECA2 are highly expressed in pollen tubes. Pollen tubes from T-DNA inserted knockout mutant lines display significant morphological defects and unique pectin deposition. Fluorescent tagging reveals organization into dynamic foci located at the lateral flanks of the pollen tube. This precisely defined subapical domain coincides which clathrin-mediated endocytosis (CME) and PIP2 localization. Using a liposome-protein binding test, we showed that AtECA2 protein and ANTH domain recombinant proteins have strong affinity to PIP2 and phosphatidic acid containing liposomes in vitro. Taken together these data suggest that Arabidopsis ANTH proteins may play an important role in CME, proper cell wall assembly and morphogenesis.

scholarly journals Recent advances in understanding how rod-like bacteria stably maintain their cell shapes

F1000Research ◽  
2018 ◽  
Vol 7 ◽  
pp. 241 ◽  
Author(s):  
Sven van Teeffelen ◽  
Lars D. Renner
Keyword(s):  
Escherichia Coli ◽  
Cell Wall ◽  
Cell Shape ◽  
Theoretical Work ◽  
Model Organisms ◽  
Mechanical Forces ◽  
Recent Developments ◽  
Cell Shapes ◽  
Shape And Size ◽  
Cell Wall Expansion

Cell shape and cell volume are important for many bacterial functions. In recent years, we have seen a range of experimental and theoretical work that led to a better understanding of the determinants of cell shape and size. The roles of different molecular machineries for cell-wall expansion have been detailed and partially redefined, mechanical forces have been shown to influence cell shape, and new connections between metabolism and cell shape have been proposed. Yet the fundamental determinants of the different cellular dimensions remain to be identified. Here, we highlight some of the recent developments and focus on the determinants of rod-like cell shape and size in the well-studied model organismsEscherichia coliandBacillus subtilis.

scholarly journals The self-organization of plant microtubules in three dimensions enable stable cortical localization and sensitivity to external cues

2017 ◽  
Author(s):  
Vincent Mirabet ◽  
Pawel Krupinski ◽  
Olivier Hamant ◽  
Elliot M Meyerowitz ◽  
Henrik Jönsson ◽  
...  
Keyword(s):  
Cell Surface ◽  
Cell Shape ◽  
Dimensional Space ◽  
Three Dimensions ◽  
Mechanical Anisotropy ◽  
Cellulose Microfibrils ◽  
Microtubule Cytoskeleton ◽  
Microtubule Network ◽  
Cell Functions ◽  
Cell Shapes

AbstractMany cell functions rely on the ability of microtubules to self-organize as complex networks. In plants, cortical microtubules are essential to determine cell shape as they guide the deposition of cellulose microfibrils, and thus control mechanical anisotropy in the cell wall. Here we analyze how, in turn, cell shape may influence microtubule behavior. Using a computational model of microtubules enclosed in a three-dimensional space, We show that the microtubule network has spontaneous configurations that could explain many experimental observations without resorting to specific regulation. In particular, we find that the preferred localization of microtubules at the cortex emerges from directional persistence of the microtubules, combined with their growth mode. We identified microtubule parameters that seem relatively insensitive to cell shape, such as length or number. In contrast, microtubule array anisotropy depends strongly on local curvature of the cell surface and global orientation follows robustly the longest axis of the cell. Lastly, we found that the network is capable of reorienting toward weak external directional cues. Altogether our simulations show that the microtubule network is a good transducer of weak external polarity, while at the same time, it easily reaches stable global configurations.Author summaryPlants exhibit an astonishing diversity in architecture and shape. A key to such diversity is the ability of their cells to coordinate and grow to reach a broad spectrum of sizes and shapes. Cell growth in plants is guided by the microtubule cytoskeleton. Here, we seek to understand how microtubules self-organize close to the cell surface. We build upon previous two-dimensional models and we consider microtubules as lines growing in three dimensions, accounting for interactions between microtubules or between microtubules and the cell surface. We show that microtubule arrays are able to adapt to various cell shapes and to reorient in response to factors such as signals or environment. Altogether, our results help to understand how the microtubule cytoskeleton contributes to the diversity of plant shapes and to how these shapes adapt to environment.

The arrangement of microtubules in leaves of monocotyledonous and dicotyledonous plants

1989 ◽  
Vol 67 (12) ◽  
pp. 3506-3512 ◽  
Author(s):  
Taizo Hogetsu
Keyword(s):  
Cell Wall ◽  
Zea Mays ◽  
Avena Sativa ◽  
Epidermal Cells ◽  
Cellulose Microfibrils ◽  
Cortical Microtubules ◽  
Monocotyledonous Plant ◽  
Pisum Sativum L ◽  
Dicotyledonous Plants ◽  
Parenchymal Cells

The first leaf of Avena sativa L., a monocotyledonous plant, grows in a region that lies within 10 mm of the base of the leaf. Cells in that region elongate longitudinally but hardly expand laterally. The orientation of cortical microtubules in the elongating region is transverse in both epidermal and parenchymal cells. The same features of the arrangement of microtubules are also observed in the leaves of Zea mays. Cellulose microfibrils in the cell wall are coaligned with microtubules, lying approximately transverse to the axis of elongation, as if they function as hoops to facilitate the longitudinal elongation of the cell. The cells of growing leaves of Pisum sativum L., a dicotyledonous plant, expand superficially in every direction at every point on the leaf. Cortical microtubules lining the outer walls of epidermal cells are arranged randomly or in parallel. The parallel microtubules are oriented in various directions. In the outer walls of epidermal cells of growing leaves, areas with different predominant orientations of microfibrils are found within a single cell, consistent with the arrangement of microtubules. These results indicate that the orientation of cortical microtubules is correlated with the orientation of microfibrils and the direction of growth in growing leaves of both monocotyledons and dicotyledons, suggesting the involvement of cortical microtubules in control of the direction of growth in leaves.

Mutant alleles of Arabidopsis RADIALLY SWOLLEN 4 and 7 reduce growth anisotropy without altering the transverse orientation of cortical microtubules or cellulose microfibrils

Development ◽  
2002 ◽  
Vol 129 (20) ◽  
pp. 4821-4830 ◽  
Author(s):  
Allison M. D. Wiedemeier ◽  
Jan E. Judy-March ◽  
Charles H. Hocart ◽  
Geoffrey O. Wasteneys ◽  
Richard E. Williamson ◽  
...  
Keyword(s):  
Mechanical Anisotropy ◽  
Cellulose Microfibrils ◽  
Analytical Determination ◽  
Temperature Sensitive ◽  
Restrictive Temperature ◽  
Permissive Temperature ◽  
Cortical Microtubules ◽  
Cell Production ◽  
Anisotropic Expansion ◽  
Anisotropic Mechanical Properties

The anisotropic growth of plant cells depends on cell walls having anisotropic mechanical properties, which are hypothesized to arise from aligned cellulose microfibrils. To test this hypothesis and to identify genes involved in controlling plant shape, we isolated mutants in Arabidopsis thaliana in which the degree of anisotropic expansion of the root is reduced. We report here the characterization of mutants at two new loci, RADIALLY SWOLLEN 4 (RSW4) and RSW7. The radial swelling phenotype is temperature sensitive, being moderate (rsw7) or negligible (rsw4) at the permissive temperature, 19°C, and pronounced at the restrictive temperature, 30°C. After transfer to 30°C, the primary root’s elongation rate decreases and diameter increases, with all tissues swelling radially. Swelling is accompanied by ectopic cell production but swelling is not reduced when the extra cell production is eliminated chemically. A double mutant was generated, whose roots swell constitutively and more than either parent. Based on analytical determination of acid-insoluble glucose, the amount of cellulose was normal in rsw4 and slightly elevated in rsw7. The orientation of cortical microtubules was examined with immunofluorescence in whole mounts and in semi-thin plastic sections, and the orientation of microfibrils was examined with field-emission scanning electron microscopy and quantitative polarized-light microscopy. In the swollen regions of both mutants, cortical microtubules and cellulose microfibrils are neither depleted nor disoriented. Thus, oriented microtubules and microfibrils themselves are insufficient to limit radial expansion; to build a wall with high mechanical anisotropy, additional factors are required, supplied in part by RSW4 and RSW7.

scholarly journals Torsions-Driven Root Helical Growth, Waving And Skewing In Arabidopsis

2021 ◽  
Author(s):  
Ke Zhou
Keyword(s):  
Cell Wall ◽  
Cellulose Microfibrils ◽  
Cross Linking ◽  
Cortical Microtubules ◽  
Root Cells ◽  
Left Handedness ◽  
Helical Growth ◽  
Root Waving ◽  
Working Together ◽  
Interesting Behavior

AbstractHelical growth broadly exists in immobile plants to support their limited movement, and Arabidopsis seedling root exhibiting natural left-handedness helical growth is considered as a simplified model for investigating this interesting behavior. Efforts have been made for understanding the mechanism of root helical growth and consequent root waving and skewing on tilted and impenetrable surface, and several models have been established. Here, previous reports are reviewed and a straightforward torsions-driven mechanism has been emphasized, and additional experiments have been performed to fill up the gaps of this theory in our study.This study implies that, torsions originating from handedness of both cortical microtubules and cellulose microfibrils play central role in root handed helical growth. Different from torsions directly provided by handed assembled cortical microtubules, torsions originating from right-handed assembled cellulose microfibrils are relaxed by their cross-linking with pectin within cell wall, but only exhibited when their cross-linking is interrupted due to damaged cell wall integrity. To topologically relax these torsions, supercoils of cortical microtubules and/or cellulose microfibrils exhibiting as oblique alignments are formed in root cells, which alter the orientation of root cell files and generate handed helical roots. Working together with gravitropic response, relaxation of torsions originating from helical roots drives roots to elongate with handedness, which therefore produces waved and skewed roots on tilted and impenetrable surface.

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