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      Mechanics of Pollen Tube Elongation: A Perspective

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          Abstract

          Pollen tube (PT) serves as a vehicle that delivers male gametes (sperm cells) to a female gametophyte during double fertilization, which eventually leads to the seed formation. It is one of the fastest elongating structures in plants. Normally, PTs traverse through the extracellular matrix at the transmitting tract after penetrating the stigma. While the endeavor may appear simple, the molecular processes and mechanics of the PT elongation is yet to be fully resolved. Although it is the most studied “tip–growing” structure in plants, several features of the structure (e.g., Membrane dynamics, growth behavior, mechanosensing etc.) are only partially understood. In many aspects, PTs are still considered as a tissue rather than a “unique cell.” In this review, we have attempted to discuss mainly on the mechanics behind PT–elongation and briefly on the molecular players involved in the process. Four aspects of PTs are particularly discussed: the PT as a cell, its membrane dynamics, mechanics of its elongation, and the potential mechanosensors involved in its elongation based on relevant findings in both plant and non-plant models.

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          Most cited references127

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          Cell movement is guided by the rigidity of the substrate.

          Directional cell locomotion is critical in many physiological processes, including morphogenesis, the immune response, and wound healing. It is well known that in these processes cell movements can be guided by gradients of various chemical signals. In this study, we demonstrate that cell movement can also be guided by purely physical interactions at the cell-substrate interface. We cultured National Institutes of Health 3T3 fibroblasts on flexible polyacrylamide sheets coated with type I collagen. A transition in rigidity was introduced in the central region of the sheet by a discontinuity in the concentration of the bis-acrylamide cross-linker. Cells approaching the transition region from the soft side could easily migrate across the boundary, with a concurrent increase in spreading area and traction forces. In contrast, cells migrating from the stiff side turned around or retracted as they reached the boundary. We call this apparent preference for a stiff substrate "durotaxis." In addition to substrate rigidity, we discovered that cell movement could also be guided by manipulating the flexible substrate to produce mechanical strains in the front or rear of a polarized cell. We conclude that changes in tissue rigidity and strain could play an important controlling role in a number of normal and pathological processes involving cell locomotion.
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            Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells.

            The mesenchymal-amoeboid transition (MAT) was proposed as a mechanism for cancer cells to adapt their migration mode to their environment. While the molecular pathways involved in this transition are well documented, the role of the microenvironment in the MAT is still poorly understood. Here, we investigated how confinement and adhesion affect this transition. We report that, in the absence of focal adhesions and under conditions of confinement, mesenchymal cells can spontaneously switch to a fast amoeboid migration phenotype. We identified two main types of fast migration--one involving a local protrusion and a second involving a myosin-II-dependent mechanical instability of the cell cortex that leads to a global cortical flow. Interestingly, transformed cells are more prone to adopt this fast migration mode. Finally, we propose a generic model that explains migration transitions and predicts a phase diagram of migration phenotypes based on three main control parameters: confinement, adhesion, and contractility. Copyright © 2015 Elsevier Inc. All rights reserved.
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              Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells.

              For more than 140 years, pollen tube guidance in flowering plants has been thought to be mediated by chemoattractants derived from target ovules. However, there has been no convincing evidence of any particular molecule being the true attractant that actually controls the navigation of pollen tubes towards ovules. Emerging data indicate that two synergid cells on the side of the egg cell emit a diffusible, species-specific signal to attract the pollen tube at the last step of pollen tube guidance. Here we report that secreted, cysteine-rich polypeptides (CRPs) in a subgroup of defensin-like proteins are attractants derived from the synergid cells. We isolated synergid cells of Torenia fournieri, a unique plant with a protruding embryo sac, to identify transcripts encoding secreted proteins as candidate molecules for the chemoattractant(s). We found two CRPs, abundantly and predominantly expressed in the synergid cell, which are secreted to the surface of the egg apparatus. Moreover, they showed activity in vitro to attract competent pollen tubes of their own species and were named as LUREs. Injection of morpholino antisense oligomers against the LUREs impaired pollen tube attraction, supporting the finding that LUREs are the attractants derived from the synergid cells of T. fournieri.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                20 October 2020
                2020
                : 11
                : 589712
                Affiliations
                [1] 1School of Life Sciences, Fujian Agriculture and Forestry University , Fuzhou, China
                [2] 2Horticultural Plant Biology and Metabolomics Center (HBMC), Fujian Agriculture and Forestry University , Fuzhou, China
                Author notes

                Edited by: Stefano Del Duca, University of Bologna, Italy

                Reviewed by: Hao Wang, South China Agricultural University, China; Lavinia Mareri, University of Siena, Italy

                *Correspondence: Ryushiro D. Kasahara, kasahara@ 123456fafu.edu.cn

                This article was submitted to Plant Cell Biology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.589712
                7606272
                33193543
                6bda6479-a917-42cf-8f74-eba7de23e061
                Copyright © 2020 Adhikari, Liu and Kasahara.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 31 July 2020
                : 30 September 2020
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 127, Pages: 13, Words: 0
                Funding
                Funded by: Fujian Agriculture and Forestry University 10.13039/501100008766
                Award ID: 114-712018008
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31970809
                Funded by: Precursory Research for Embryonic Science and Technology 10.13039/501100009023
                Award ID: 13416724
                Categories
                Plant Science
                Review

                Plant science & Botany
                mechanosensors,tip elongation,durotaxis,kiss–and–run,callus plug,pollen tube

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