The cytoskeleton in plant and fungal cell tip growth

Geitmann, Anja; Emons, A.M.C.

doi:10.1046/j.1365-2818.2000.00702.x

Cited by 181 publications

(140 citation statements)

References 315 publications

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“…Two possible mechanisms of intrusive growth are cell elongation by growth of the very cell tip-cell tip growth-, and cell elongation by growth along the surface of the entire cell-diffuse growth. Tip growing cells are characterized by specific cytoplasmic zones at the very tip (Geitmann and Emons 2000), and longitudinally aligned microfilaments (Ketelaar et al , 2003 and longitudinally aligned microtubules (Sieberer et al 2002) in the subapical region, whereas cells with diffuse growth do not show such organization. The study on the mechanism of intrusive growth is hampered by the inability to reproduce it in vitro or to isolate the cells at this stage of development in sufficient amounts for biochemical or molecular-biological study.…”

Section: Introductionmentioning

confidence: 99%

Intrusive growth of flax phloem fibers is of intercalary type

Ageeva

Petrovská

Kieft

et al. 2005

Planta

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Flax (Linum usitatissimum L.) phloem fibers elongate considerably during their development and intrude between existing cells. We questioned whether fiber elongation is caused by cell tip growth or intercalary growth. Cells with tip growth are characterized by having two specific zones of cytoplasm in the cell tip, one with vesicles and no large organelles at the very tip and one with various organelles amongst others longitudinally arranged cortical microtubules in the subapex. Such zones were not observed in elongating flax fibers. Instead, organelles moved into the very tip region, and cortical microtubules showed transversal and helical configurations as known for cells growing in intercalary way. In addition, pulse-chase experiments with Calcofluor White resulted in a spotted fluorescence in the cell wall all over the length of the fiber. Therefore, it is concluded that fiber elongation is not achieved by tip growth but by intercalary growth. The intrusively growing fiber is a coenocytic cell that has no plasmodesmata, making the fibers a symplastically isolated domain within the stem.

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Section: Introductionmentioning

confidence: 99%

Intrusive growth of flax phloem fibers is of intercalary type

Ageeva

Petrovská

Kieft

et al. 2005

Planta

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“…Building cellularscale structures with the correct spatial architecture and mechanical properties requires that nanometer-scale proteins have the ability to detect and alter cell shape across multiple length scales. In walled organisms such as plants (1)(2)(3)(4)(5), fungi (6), and bacteria (7)(8)(9)(10), morphogenesis is often achieved through an interplay between the cytoskeleton and cell wall synthesis. A central challenge in bacterial physiology is to understand the feedback between cell shape and the coordination of wall growth by the cytoskeleton.…”

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confidence: 99%

Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization

Ursell

Nguyen

Monds

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

234

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Cells typically maintain characteristic shapes, but the mechanisms of self-organization for robust morphological maintenance remain unclear in most systems. Precise regulation of rod-like shape in Escherichia coli cells requires the MreB actin-like cytoskeleton, but the mechanism by which MreB maintains rod-like shape is unknown. Here, we use time-lapse and 3D imaging coupled with computational analysis to map the growth, geometry, and cytoskeletal organization of single bacterial cells at subcellular resolution. Our results demonstrate that feedback between cell geometry and MreB localization maintains rod-like cell shape by targeting cell wall growth to regions of negative cell wall curvature. Pulsechase labeling indicates that growth is heterogeneous and correlates spatially and temporally with MreB localization, whereas MreB inhibition results in more homogeneous growth, including growth in polar regions previously thought to be inert. Biophysical simulations establish that curvature feedback on the localization of cell wall growth is an effective mechanism for cell straightening and suggest that surface deformations caused by cell wall insertion could direct circumferential motion of MreB. Our work shows that MreB orchestrates persistent, heterogeneous growth at the subcellular scale, enabling robust, uniform growth at the cellular scale without requiring global organization.bacterial cytoskeleton | biophysical modeling | morphogenesis H ow cells maintain stable and defined morphologies is a fundamental question in all branches of life. Building cellularscale structures with the correct spatial architecture and mechanical properties requires that nanometer-scale proteins have the ability to detect and alter cell shape across multiple length scales. In walled organisms such as plants (1-5), fungi (6), and bacteria (7-10), morphogenesis is often achieved through an interplay between the cytoskeleton and cell wall synthesis. A central challenge in bacterial physiology is to understand the feedback between cell shape and the coordination of wall growth by the cytoskeleton.The cell wall plays a critical mechanical role in balancing turgor stress in virtually all bacteria and is both necessary and sufficient to define cell shape (11). The bacterial cell wall is a mesh-like network of sugar strands cross-linked by peptides (11,12). In rod-shaped Escherichia coli cells, cell wall growth occurs along the cylindrical body. Biophysical modeling has suggested that a random pattern of insertion cannot preserve cell shape (13), indicating that spatial coordination of the growth machinery is necessary for cell shape maintenance. Several lines of evidence demonstrate that the actin homolog MreB (14, 15) plays a major role in this coordination in most rod-shaped bacteria. The small molecule A22 depolymerizes MreB and causes a gradual transition from a rod-like to a spherical shape (15)(16)(17). This observation suggests that the disruption of MreB changes the patterning of new material insertion, although the nature of this...

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“…The elongation of the pollen tube, as well as that of animal axons, plant root hairs, fungal hyphae, and moss protonema, is achieved by a polarized mode of growth, termed tip growth (FranklinTong, 1999;Palanivelu and Preuss, 2000;Hepler et al, 2001), which involves the tip-localized exocytosis of Golgi-derived vesicles containing cell wall precursors (Franklin-Tong, 1999). The tip of the pollen tube is devoid of organelles, but contains almost exclusively Golgi-derived vesicles (Geitmann and Emons, 2000). In the shank of the tubes, an inverse fountain pattern of cytoplasmic streaming is observed; organelles and vesicles are transported toward the apex in the cortical region and basipetally in the central cytoplasm (Pierson et al, 1990).…”

mentioning

confidence: 99%

The Putative Arabidopsis Homolog of Yeast Vps52p Is Required for Pollen Tube Elongation, Localizes to Golgi, and Might Be Involved in Vesicle Trafficking

et al. 2004

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The screening of the Versailles collection of Arabidopsis T-DNA transformants allowed us to identify several male gametophytic mutants, including poky pollen tube (pok). The pok mutant, which could only be isolated as a hemizygous line, exhibits very short pollen tubes, explaining the male-specific transmission defect observed in this line. We show that the POK gene is duplicated in the Arabidopsis genome and that the predicted POK protein sequence is highly conserved from lower to higher eukaryotes. The putative POK homolog in yeast (Saccharomyces cerevisiae), referred to as Vps52p/SAC2, has been shown to be located at the late Golgi and to function in a complex with other proteins, Vps53p, Vps54p, and Vps51p. This complex is involved in retrograde trafficking of vesicles between the early endosomal compartment and the trans-Golgi network. We present the expression patterns of the POK gene and its duplicate P2 in Arabidopsis, and of the putative Arabidopsis homologs of VPS53 and VPS54 of yeast. We show that a POK::GFP fusion protein localizes to Golgi in plant cells, supporting the possibility of a conserved function for Vps52p and POK proteins. These results, together with the expression pattern of the POK::GUS fusion and the lack of plants homozygous for the pok mutation, suggest a more general role for POK in polar growth beyond the pollen tube elongation process.Pollen tube growth is a vital process during male gametophyte development, since it allows male gametes to reach the ovules and achieve fertilization (Preuss, 1995). The elongation of the pollen tube, as well as that of animal axons, plant root hairs, fungal hyphae, and moss protonema, is achieved by a polarized mode of growth, termed tip growth (FranklinTong, 1999;Palanivelu and Preuss, 2000;Hepler et al., 2001), which involves the tip-localized exocytosis of Golgi-derived vesicles containing cell wall precursors (Franklin-Tong, 1999). The tip of the pollen tube is devoid of organelles, but contains almost exclusively Golgi-derived vesicles (Geitmann and Emons, 2000). In the shank of the tubes, an inverse fountain pattern of cytoplasmic streaming is observed; organelles and vesicles are transported toward the apex in the cortical region and basipetally in the central cytoplasm (Pierson et al., 1990). Actin filaments and microtubules, which are organized in longitudinal arrays more or less parallel to the elongation axis, act as tracks for cytoplasmic streaming and allow delivery of vesicles to the tip (Pierson et al., 1990;Vidali and Hepler, 2001). The use of membrane structure dyes, such as FM1-43 or FM4-64 (Parton et al., 2001;Camacho and Malhó , 2003), has revealed dynamic endo/ exocytosis processes at the tip of the pollen tube, but the molecular events underlying these processes are still poorly understood. The recent identification of the Golgi-associated tobacco (Nicotiana tabacum), Rab GTPase NtRab2, predominantly expressed in pollen, suggests that tip growth and vesicle trafficking could be tightly linked (Cheung et al., 2002). Moreover, a...

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The cytoskeleton in plant and fungal cell tip growth

Cited by 181 publications

References 315 publications

Intrusive growth of flax phloem fibers is of intercalary type

Intrusive growth of flax phloem fibers is of intercalary type

Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization

The Putative Arabidopsis Homolog of Yeast Vps52p Is Required for Pollen Tube Elongation, Localizes to Golgi, and Might Be Involved in Vesicle Trafficking

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