Dynamic changes in the organization of microfilaments associated with the photocontrolled motility of chloroplasts in epidermal cells ofVattisneria

Dong, Xia-Jing; Ryu, Jung‐Hwa; Takagi, Shingo; Nagai, Reiko

doi:10.1007/bf01279183

Cited by 48 publications

(42 citation statements)

References 16 publications

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“…For example, in Arabidopsis, baskets of actin filaments have been observed surrounding the chloroplasts, and disruption of these filaments by latrunculin B resulted in a disorganization of the intracellular arrangement of chloroplasts (Kandasamy and Meagher, 1999). Similarly, the intracellular movement of chloroplasts in many cells, including algae, mosses, ferns, and angiosperms, has been shown to be inhibited by antiactin drugs (Witztum and Parthasarathy, 1985;Menzel and Schliwa, 1986;Kadota and Wada, 1992;Nagai, 1993;Dong et al, 1996;Sato et al, 2001). These studies suggest that actin filaments play a major role in the positioning and movement of chloroplasts.…”

Section: Discussionmentioning

confidence: 99%

The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C4 Photosynthesis in Chenopodiaceae Species

2006

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Recently, three Chenopodiaceae species, Bienertia cycloptera, Bienertia sinuspersici, and Suaeda aralocaspica, were shown to possess novel C 4 photosynthesis mechanisms through the compartmentalization of organelles and photosynthetic enzymes into two distinct regions within a single chlorenchyma cell. Bienertia has peripheral and central compartments, whereas S. aralocaspica has distal and proximal compartments. This compartmentalization achieves the equivalent of spatial separation of Kranz anatomy, including dimorphic chloroplasts, but within a single cell. To characterize the mechanisms of organelle compartmentalization, the distribution of the major organelles relative to the cytoskeleton was examined. Examination of the distribution of the cytoskeleton using immunofluorescence studies and transient expression of green fluorescent protein-tagged cytoskeleton markers revealed a highly organized network of actin filaments and microtubules associating with the chloroplasts and showed that the two compartments in each cell had different cytoskeletal arrangements. Experiments using cytoskeleton-disrupting drugs showed in Bienertia and S. aralocaspica that microtubules are critical for the polarized positioning of chloroplasts and other organelles. Compartmentalization of the organelles in these species represents a unique system in higher plants and illustrates the degree of control the plant cell has over the organization and integration of multiorganellar processes within its cytoplasm.

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Section: Discussionmentioning

confidence: 99%

The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C4 Photosynthesis in Chenopodiaceae Species

2006

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“…Probably, it is functionally related to plastid distribution, a hypothesis made about other cells types (Dong et al, 1996, and literature therein). Actin filaments related to plastid surface have been observed in GCs and GC mother cells of Selaginella (Cleary et al, 1992(Cleary et al, , 1993.…”

Section: Actin Filament Organization In Differentiating Guard Cellsmentioning

confidence: 94%

Microtubule and actin filament organization during stomatal morphogenesis in the fern Asplenium nidus. II. Guard cells

Apostolakos

Galatis

1999

New Phytologist

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The post-cytokinetic guard cells of Asplenium nidus display a prominent perinuclear microtubule system and a few microtubules under the periclinal walls. Afterwards, microtubules appear on the whole surface of the ventral wall, whereas those below the periclinal walls proliferate and tend to become parallel with the ventral wall. The perinuclear microtubules gradually diminish but persist in later stages of guard cell differentiation. In postcytokinetic guard cells, actin is found in the perinuclear cytoplasm and in the cortical cytoplasm lining all the walls. In differentiating guard cells, the following cortical microtubules and actin filament ' systems ' appear in succession : (a) radial microtubule and actin filament arrays beneath the periclinal walls converging on the stomatal pore region, (b) anticlinal microtubule bundles, which are co-localized with actin filaments, along the ventral wall outlining the region of the stomatal pore, (c) periclinal microtubules and actin filaments on the polar ventral wall ends. These cytoskeletal systems, except for the radial actin filaments, persist in advanced stages of guard cell differentiation. Instead of the radial actin filaments, a prominent actin filament reticulum is organized under the margins of the developing wall thickenings of the stomatal pore. In addition, an extensive endoplasmic actin filament reticulum develops around the plastids. It seems likely that the successive microtubule systems in guard cells are formed by putative microtubule organizing centres operating in a definite spatial and temporal succession. Guard cell morphogenesis is the outcome of a definite process, in which the cortical microtubule cytoskeleton plays the primary role, implicated in the deposition of cellulose microfibrils and probably of the local wall thickenings. Callose or a callose-like glucan is deposited on the whole surface of the nascent ventral wall and in the wall regions where thickenings are deposited. Finally, the guard cells of Asplenium assume a kidney shape and display polar hypostomatic swellings. Particular structural features established in guard cell mother cells affect guard cell morphogenesis.

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“…Chloroplast movement in the green alga Dichotomosiphon is microtubuledependent (Maekawa and Nagai 1988); however, chloroplasts that accumulated in cell apices after photo-orientation movement were found to be associated with numerous fine bundles of actin filaments (Fig.·2). Also, in vascular plants, actin filaments surrounding chloroplasts have frequently been observed by light microscopy (Kobayashi et al, 1987;Kadota and Wada, 1992a;Dong et al, 1996;Kandasamy and Meagher, 1999). In A. thaliana, disruption of the actin filaments by the anti-actin drug latrunculin B led to the disruption of the intracellular arrangement of chloroplasts (Kandasamy and Meagher, 1999).…”

Section: ) and The Angiosperm Lily (Lilium Longiflorum;mentioning

confidence: 99%

Actin-based photo-orientation movement of chloroplasts in plant cells

Takagi

2003

Journal of Experimental Biology

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SUMMARYIn photosynthesizing plant cells, chloroplasts change their arrangements and/or positions in response to light irradiation. These photo-orientation movements of chloroplasts are believed to play important roles in optimizing the photosynthetic activity of plant cells. We have been investigating the roles of the actin cytoskeleton in the intracellular movement and positioning of chloroplasts using the aquatic monocot Vallisneria giganteaGraebner and the terrestrial dicot Spinacia oleracea L. (spinach). In Vallisneria epidermal cells, chloroplasts accumulate on the cytoplasmic layer facing the top surface (outer periclinal layer) under dim red light, whereas they move to the cytoplasmic layer perpendicular to the outer periclinal layer (anticlinal layer) under strong blue light. Concomitant with these responses, actin filaments exhibit dramatic changes in their configurations. The possible modes of action of the actin cytoskeleton to regulate the movement and positioning of chloroplasts are briefly summarized,together with our recent analysis of the association of actin filaments with chloroplasts isolated from spinach leaves.

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Dynamic changes in the organization of microfilaments associated with the photocontrolled motility of chloroplasts in epidermal cells ofVattisneria

Cited by 48 publications

References 16 publications

The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C4 Photosynthesis in Chenopodiaceae Species

The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C4 Photosynthesis in Chenopodiaceae Species

Microtubule and actin filament organization during stomatal morphogenesis in the fern Asplenium nidus. II. Guard cells

Actin-based photo-orientation movement of chloroplasts in plant cells

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