Reactions to light in Volvox, with special reference to the process of orientation

Mast, S. O.

doi:10.1007/bf00342378

Cited by 25 publications

(25 citation statements)

References 14 publications

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“…Details are given in Materials and Methods and SI Text. High-speed imaging of flagella revealed, in accord with proposals by several investigators (13)(14)(15), that the somatic cells change their beating frequency rather than their beating direction (17). Instead of quantifying the average photoresponse by recording the beating frequency of each flagellum of every somatic cell, we measured the fluid motion produced by the flagellar beating by using particle image velocimetry (PIV).…”

Section: Resultsmentioning

confidence: 55%

Fidelity of adaptive phototaxis

Drescher

Goldstein

Tuval

2010

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

141

145

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Along the evolutionary path from single cells to multicellular organisms with a central nervous system are species of intermediate complexity that move in ways suggesting high-level coordination, yet have none. Instead, organisms of this type possess many autonomous cells endowed with programs that have evolved to achieve concerted responses to environmental stimuli. Here experiment and theory are used to develop a quantitative understanding of how cells of such organisms coordinate to achieve phototaxis, by using the colonial alga Volvox carteri as a model. It is shown that the surface somatic cells act as individuals but are orchestrated by their relative position in the spherical extracellular matrix and their common photoresponse function to achieve colony-level coordination. Analysis of models that range from the minimal to the biologically faithful shows that, because the flagellar beating displays an adaptive down-regulation in response to light, the colony needs to spin around its swimming direction and that the response kinetics and natural spinning frequency of the colony appear to be mutually tuned to give the maximum photoresponse. These models further predict that the phototactic ability decreases dramatically when the colony does not spin at its natural frequency, a result confirmed by phototaxis assays in which colony rotation was slowed by increasing the fluid viscosity.adaptation | evolution | flagella | fluid dynamics | multicellularity

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Section: Resultsmentioning

confidence: 55%

Fidelity of adaptive phototaxis

Drescher

Goldstein

Tuval

2010

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

141

145

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“…The older literature contains reports of no change in the speed of movement, or orthophotokinesis, by phytoflagellates with light intensity change (Mainx, 1929;Mast and Graves, 1922) as well as reports of definite change with intensity (Mainx and Wolf, 1939;Holmes, 1903;Oltman, 1917;Mast, 1926;Luntz, 1931aLuntz, ,b, 1932. More recently, using Euglena, Wolken and Shin (1958) found that orthophotokinesis increased independent of phototaxis when ambient white light was changed from 2 to 40 fc.…”

Section: Photokinesismentioning

confidence: 95%

Light and Diurnal Vertical Migration: Photobehavior and Photophysiology of Plankton

ForwardJr.

1976

Photochemical and Photobiological Reviews

116

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“…However, how flagella activity in the anteriormost cells actually modulates colonial steering is less certain. One suggestion is that for positive phototaxis the anterior cells on the illuminated side of the colony cease beating, while cells on the other side remain beating or may even accelerate (Mast 1911, Huth 1970, Hand and Haupt 1971, Sakaguchi and Iwasa 1979, Sakaguchi and Tawada 1977. As the colony rotates, new cells will be exposed to the illuminated side and temporarily stop beating while those that have rotated onto the dark side will resume beating again.…”

Section: Colonial Construction and Colonial Steeringmentioning

confidence: 97%

“…However, the arguments of Mast (1926), who favored the variable-beat-direction model, seem to be convincing. In fact, Mast (1911) had originally favored the variable-frequency model but came to accept the variable-beat-direction model based on the behavior of colonies exposed to step-up and step-down responses. Mast reported that positively phototactic colonies increased their rate of rotation and decreased their forward velocity after a step-up response.…”

Section: Colonial Construction and Colonial Steeringmentioning

confidence: 98%

“…Instead, the colonial turning is probably the result of cells at the appropriate portions of the colony behaving differently. Several lines of evidence suggest that the cells at the anterior of the colony are involved in the modulation of activity that results in steering (Mast 1911(Mast , 1926Huth 1970, Hand andHaupt 1971;Sakaguchi and Tawada 1977;Sakaguchi and Iwasa 1979). However, how flagella activity in the anteriormost cells actually modulates colonial steering is less certain.…”

Section: Colonial Construction and Colonial Steeringmentioning

confidence: 98%

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Motility in the colonial and multicellular Volvocales: structure, function, and evolution

Hoops

1997

Protoplasma

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Summary. The colonial Volvocales are often said to be composed of Chlamydomonas-like cells, but there are substantial differences in motility and flagellar apparatus construction between the unicellular forms and the individual members of a colony or spheroid. These changes appear to be required for effective organismal motion and might possibly limit the rate at which new colonial forms evolve from unicellular ones. The flagellar-beat envelopes in colonial members are modified such that they beat in the same direction and in parallel planes with their effective strokes at right angles to the cellular anterior-posterior axis. These changes result from a series of developmental events of the flagellar apparatus of the colonial forms while the colony is still an embryo. Differences in the flagellar-apparatus structure in the members of the Goniaceae and Volvocaceae are not obviously correlated with the traditional placement of these algae in a simple volvocine lineage. Effective colonial motion clearly requires precise positioning and rotational orientation of the cells within the colony. Almost any arrangement where the cells are placed with rotational symmetry within the colony results in colonial progression with rotation. Such rotational symmetry is present from the time of embryogenesis. The mechanism that leads to organismal steering in behavioral responses (e.g., phototaxis) must likewise differ between colonial and unicellular forms. In at least some cases, this appears to result from changes in beat frequency in some parts of the spheroid, but changes in beat direction cannot be ruled out for all forms.

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Reactions to light in Volvox, with special reference to the process of orientation

Cited by 25 publications

References 14 publications

Fidelity of adaptive phototaxis

Fidelity of adaptive phototaxis

Light and Diurnal Vertical Migration: Photobehavior and Photophysiology of Plankton

Motility in the colonial and multicellular Volvocales: structure, function, and evolution

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