A physical perspective on cytoplasmic streaming - PubMed (original) (raw)

A physical perspective on cytoplasmic streaming

Raymond E Goldstein et al. Interface Focus. 2015.

Abstract

Organisms show a remarkable range of sizes, yet the dimensions of a single cell rarely exceed 100 µm. While the physical and biological origins of this constraint remain poorly understood, exceptions to this rule give valuable insights. A well-known counterexample is the aquatic plant Chara, whose cells can exceed 10 cm in length and 1 mm in diameter. Two spiralling bands of molecular motors at the cell periphery drive the cellular fluid up and down at speeds up to 100 µm s(-1), motion that has been hypothesized to mitigate the slowness of metabolite transport on these scales and to aid in homeostasis. This is the most organized instance of a broad class of continuous motions known as 'cytoplasmic streaming', found in a wide range of eukaryotic organisms-algae, plants, amoebae, nematodes and flies-often in unusually large cells. In this overview of the physics of this phenomenon, we examine the interplay between streaming, transport and cell size and discuss the possible role of self-organization phenomena in establishing the observed patterns of streaming.

Keywords: cell size; cytoplasmic streaming; transport.

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Figures

Figure 1.

Figure 1.

Molecular crowding in eukaryotic cytoplasm. Shown is an illustration of the contents of the yeast Saccharomyces cerevisiae. Proteins, ribosomes with mRNA, microtubules, actin filaments and intermediate filaments are all drawn to scale and at physiological concentrations. (Adapted with permission from [18].)

Figure 2.

Figure 2.

Topologies of cytoplasmic streaming. (a) Rotational streaming in internodal cells of Chara corallina. (b) A developing oocyte of Drosophila exhibits a correlated random flow field with typical flow rates of a few to tens of nanometres per second. Schematic of the velocity field, extracted by particle image velocimetry. (c) Circulation streaming in the periphery and transvacuolar strand of epidermal cells, e.g. as found in the root of Medicago truncatula [72]. (d) Reverse-fountain streaming in Lilium longiflorum (left) and Nicotiana tabacum (right). (Image modified from [73].) (e) Periodic shuttle streaming in plasmodium fragments of Physarum polycephalum. (Adapted from [63].)

Figure 3.

Figure 3.

Rotational streaming in the characean algae. (a) A shoot of Chara corallina anchored in agar. Single-celled internodes connect nodal complexes where a whorl of six branchlets is formed. (b) Cytoplasmic streaming takes place along two domains shaped as spiralling bands. (c) This circulation is driven by the motion of myosin molecular motors along bundled actin filaments. This image shows a merged stack of confocal slices, with the colours denoting the focal position. Actin bundles can be observed below chloroplast rows at the surface of the cell. (Image courtesy S. Ganguly.) (d) The motion of myosin at the periphery entrains the outer layer of cytoplasm, which is of order 10 µm in thickness. The two moving bands are separated by a neutral line visible as a row of missing chloroplasts. The motion at the wall induces a shear flow in the central vacuole of the cell.

Figure 4.

Figure 4.

Hydrodynamic prediction and MRV measurements of vacuolar flow. (a) The internodal flow has a helical symmetry: an invariance under a translation along the longitudinal axis combined with a rotation. The two axes that naturally follow from this symmetry are the vector e H, which points along the bands, and the vector e φ , which is orthogonal to the bands. (b) Theoretically predicted flow field along the e H component, showing the vacuolar shear profile. (c) The e r and e φ components reveal a small secondary circulation along the centre of the cell. (d) MRI scan of an internode placed in a glass tube, with spiralling lines indicating positions of the neutral line, and coloured bands showing the domains used for velocity measurements. (e) Velocity profiles measured at each of the domains show excellent agreement with the theoretical profile. (Figures modified from [–116].)

Figure 5.

Figure 5.

Self-organization of cytoplasmic streaming in a mathematical model of Chara [174]. Colour coding corresponds to the _z_-component of an order parameter associated with actin filaments at the periphery, and white lines represent indifferent zones separating up- and down-streaming regions. Superimposed are streamlines of the cytoplasmic flow induced by the filament field, where the flow is directed from the thin end to the thick end of the individual lines. Panels show progression from random disorder through local order to complete steady cyclosis.

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