Oriented movement of statoliths studied in a reduced gravitational field during parabolic flights of rockets

Volkmann, Dieter; Buchen, Brigitte; Hejnowicz, Z.; Tewinkel, Martin; Sievers, Andreas

doi:10.1007/bf00194056

Cited by 103 publications

(43 citation statements)

References 26 publications

(31 reference statements)

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“…The number of statoliths (50-60 per cell) observed in SW rhizoids is similar to values previously reported in the literature for mature Chara rhizoids (generated from thallus cuttings) grown in either Foresburg medium (which is a more enriched medium than APW) or agar without any nutrients (Sievers, 1971;Sievers and Volkmann, 1979;Hejnowicz and Sievers, 1981;Bartnik and Sievers, 1988;Volkmann et al ;1991;Braun and Sievers, 1993). However, several studies have demonstrated that immature, developing Chara rhizoids contain fewer statoliths than do mature rhizoids (Schroter et al, 1973;Kiss, 1992).…”

Section: Discussionsupporting

confidence: 85%

The Response to Gravity Is Correlated with the Number of Statoliths in Chara Rhizoids

Kiss

1994

Plant Physiol.

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In contrast to higher plants, Chara rhizoids have single membrane-bound compartments that appear to function as statoliths. Rhizoids were generated by germinating zygotes of Chara in either soil water (SW) medium or artificial pond water (APW) medium. Differential-interference-contrast microscopy demonstrated that rhizoids from SW-grown plants typically contain 50 to 60 statoliths per cell, whereas rhizoids from APW-grown plants contain 5 to 10 statoliths per cell. Rhizoids from SW are more responsive to gravity than rhizoids from APW because (a) SW rhizoids were oriented to gravity during vertical growth, whereas APW rhizoids were relatively disoriented, and (b) curvature of SW rhizoids was 3 to 4 times greater throughout the time course of curvature. l h e growth rate of APW rhizoids was significantly greater than that of SWgrown rhizoids. This latter result suggests that APW rhizoids are not limited in their ability for gravitropic curvature by growth and that these rhizoids are impaired in the early stages of gravitropism (i.e. gravity perception). Plants grown in APW appeared to be healthy because of their growth rate and the vigorous cytoplasmic streaming observed in the rhizoids. This study is comparable to earlier studies of gravitropism in starch-deficient mutants of higher plants and provides support for the role of statoliths in gravity perception.Gravitropism in plants has been divided into the following stages: perception, transduction, and response, i.e. differentia1 growth leading to curvature (Evans et al., 1986). The perception of gravity is generally thought to involve statoliths, which are dense, movable intracellular particles (Salisbury, 1993).In higher-plant roots and shoots, a great deal of evidence supports the hypothesis that amyloplasts serve as statoliths. This evidence includes the observation that starch-deficient plants have a weaker graviresponse compared to plants with the normal leve1 of starch (Hertel et al., 1969;Iversen, 1969; Sack and Kiss, 1989; Sack 1991). In these studies, starch deficiency was induced by treatment (e.g. applied chemicals, darkness) or mutation. Two particularly valuable mutants in plant gravitropism studies have been a starchless mutant of Arabidopsis and a low-starch mutant of Nicotiana that are deficient in the activity of the enzyme phosphoglucomutase Sack, 1989, 1990 relative to their respective wild types, yet they have greatly reduced gravitropic sensitivity. In contrast to those in higher plants, the presumed statoliths in rhizoids of the alga Chara are barium-and sulfurcontaining vesicles that are located near the apex of the rhizoid and that settle to the lower cell wall within minutes after horizontal reorientation (Sievers and Volkmann, 1979; Sievers and Schnepf, 1981). When these vesicles are centrifuged from the apex of the rhizoid, growth continues but the rhizoids do not respond to gravity (Buder, 1961). Following regeneration of these vesicles at the apex, the rhizoid again becomes graviresponsive. These and other observations (eg. ...

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Section: Discussionsupporting

confidence: 85%

The Response to Gravity Is Correlated with the Number of Statoliths in Chara Rhizoids

Kiss

1994

Plant Physiol.

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“…There are several reports indicating that the actomyosin system is involved in the positioning of statoliths and in the modulation of the sedimentation process in order to meet specific requirements for a most beneficial gravitropic response (Sievers et al, 1991a;Volkmann et al, 1991Volkmann et al, , 1999Driss-Ecole et al, 2000;Perbal et al, 2004). Although the kinetics of statolith movements have been analyzed in gravisensing cells of shoots (Sack et al, 1984;Saito et al, 2005) and roots (Sack et al, 1985(Sack et al, , 1986MacCleery and Kiss, 1999;Yoder et al, 2001), interpretation of the results with respect to gravity sensing is difficult because the interaction between statoliths and the cytoskeleton and its role in the graviperception mechanism is far from being understood in these cell types.…”

Section: Gravisensitivity Is Determined By Molecular Interactions Betmentioning

confidence: 99%

How to Activate a Plant Gravireceptor. Early Mechanisms of Gravity Sensing Studied in Characean Rhizoids during Parabolic Flights

et al. 2005

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Early processes underlying plant gravity sensing were investigated in rhizoids of Chara globularis under microgravity conditions provided by parabolic flights of the A300-Zero-G aircraft and of sounding rockets. By applying centrifugal forces during the microgravity phases of sounding rocket flights, lateral accelerations of 0.14g, but not of 0.05g, resulted in a displacement of statoliths. Settling of statoliths onto the subapical plasma membrane initiated the gravitropic response. Since actin controls the positioning of statoliths and restricts sedimentation of statoliths in these cells, it can be calculated that lateral actomyosin forces in a range of 2 3 10 214 N act on statoliths to keep them in place. These forces represent the threshold value that has to be exceeded by any lateral acceleration stimulus for statolith sedimentation and gravisensing to occur. When rhizoids were gravistimulated during parabolic plane flights, the curvature angles of the flight samples, whose sedimented statoliths became weightless for 22 s during the 31 microgravity phases, were not different from those of in-flight 1g controls. However, in ground control experiments, curvature responses were drastically reduced when the contact of statoliths with the plasma membrane was intermittently interrupted by inverting gravistimulated cells for less than 10 s. Increasing the weight of sedimented statoliths by lateral centrifugation did not enhance the gravitropic response. These results provide evidence that graviperception in characean rhizoids requires contact of statoliths with membrane-bound receptor molecules rather than pressure or tension exerted by the weight of statoliths.

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“…Any deviation from the vertical growth direction, however, causes statoliths to sediment onto a specific gravisensitive area of the subapical cell flank, thereby initiating the gravitropic curvature response. Abolishing the gravity force results in an axial displacement of statoliths away from the cell tip (Volkmann et al 1991;Buchen et al 1993;Braun et al 2002). Data on the dynamics of this movement of statoliths is available from various real μg conditions like parabolic plane flights, sounding rocket missions (TEXUS, MAXUS) and several space shuttle missions (Bunchen et al 1991(Bunchen et al , 1993Volkmann et al 1991;Braun et al 2002;Limbach et al 2005).…”

Section: Introductionmentioning

confidence: 99%

“…Abolishing the gravity force results in an axial displacement of statoliths away from the cell tip (Volkmann et al 1991;Buchen et al 1993;Braun et al 2002). Data on the dynamics of this movement of statoliths is available from various real μg conditions like parabolic plane flights, sounding rocket missions (TEXUS, MAXUS) and several space shuttle missions (Bunchen et al 1991(Bunchen et al , 1993Volkmann et al 1991;Braun et al 2002;Limbach et al 2005). Chara rhizoids which have already been studied on 2D-and 3D clinostats (Cai et al 1997;Hoson et al 1997;Braun et al 2002) showed similar effects like in real microgravity.…”

Section: Introductionmentioning

confidence: 99%

Analysis of Statoliths Displacement in Chara Rhizoids for Validating the Microgravity-Simulation Quality of Clinorotation Modes

Krause

Braun

Hauslage

et al. 2018

Microgravity Sci. Technol.

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In single-celled rhizoids of the green algae Chara, positively gravitropic growth is governed by statoliths kept in a dynamically stable position 10-25 μm above the cell tip by a complex interaction of gravity and actomyosin forces. Any deviation of the tube-like cells from the tip-downward orientation causes statoliths to sediment onto the gravisensitive subapical cell flank which initiates a gravitropic curvature response. Microgravity experiments have shown that abolishing the net tip-directed gravity force results in an actomyosin-mediated axial displacement of statoliths away from the cell tip. The present study was performed to critically assess the quality of microgravity simulation provided by different operational modes of a Random Positioning Machine (RPM) running with one axis (2D mode) or two axes (3D mode) and different rotational speeds (2D), speed ranges and directions (3D). The effects of 2D and 3D rotation were compared with data from experiments in real microgravity conditions (MAXUS sounding rocket missions). Rotational speeds in the range of 60-85 rpm in 2D and 3D modes resulted in a similar kinetics of statolith displacement as compared to real microgravity data, while slower clinorotation (2-11 rpm) caused a reduced axial displacement and a more dispersed arrangement of statoliths closer to the cell tip. Increasing the complexity of rotation by adding a second rotation axis in case of 3D clinorotation did not increase the quality of microgravity simulation, however, increased side effects such as the level of vibrations resulting in a more dispersed arrangement of statoliths. In conclusion, fast 2D clinorotation provides the most appropriate microgravity simulation for investigating the graviperception mechanism in Chara rhizoids, whereas slower clinorotation speeds and rotating samples around two axes do not improve the quality of microgravity simulation.

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Oriented movement of statoliths studied in a reduced gravitational field during parabolic flights of rockets

Cited by 103 publications

References 26 publications

The Response to Gravity Is Correlated with the Number of Statoliths in Chara Rhizoids

The Response to Gravity Is Correlated with the Number of Statoliths in Chara Rhizoids

How to Activate a Plant Gravireceptor. Early Mechanisms of Gravity Sensing Studied in Characean Rhizoids during Parabolic Flights

Analysis of Statoliths Displacement in Chara Rhizoids for Validating the Microgravity-Simulation Quality of Clinorotation Modes

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