Cellular differentiation in Pleodorina californica.

Kikuchi, Kazuko

doi:10.1508/cytologia.43.153

Cited by 13 publications

(17 citation statements)

References 2 publications

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“…Another essential step towards multicellularity was the evolution of a mechanism for cell sheet folding, which is required in multicellular volvocine embryos to turn themselves right-side out at the end of embryogenesis and to expose their flagella. This process, in which the orientation of the cell sheet is reversed and the embryos achieve their adult configuration, is called ‘inversion.’ After the completion of the cell division phase and before inversion, the embryos of Gonium [ 18 , 26 ] , Pandorina [ 37 , 38 ] , Eudorina [ 16 , 38 ] and Pleodorina [ 20 ] consist of a bowl-shaped cell sheet, whereas the embryonic cells of Volvox [ 38 , 39 ] form a spherical cell sheet. With exception of the genus Astrephomene [ 40 – 42 ], all multicellular volvocine embryos face the same “problem”: the flagellar ends of all the cells point toward the interior of the bowl-shaped or spherical cell sheet rather than to the exterior, where they need to be later to function during locomotion.…”

Section: Introductionmentioning

confidence: 99%

“…With exception of the genus Astrephomene [ 40 – 42 ], all multicellular volvocine embryos face the same “problem”: the flagellar ends of all the cells point toward the interior of the bowl-shaped or spherical cell sheet rather than to the exterior, where they need to be later to function during locomotion. The correction of this awkward situation by inversion has been investigated in some multicellular volvocine genera with different degrees of detail [ 4 , 16 – 18 , 20 , 23 , 37 – 39 , 43 – 54 ].…”

Section: Introductionmentioning

confidence: 99%

“…2b, c ). Therefore, species like Pandorina , Eudorina and Pleodorina show a complete inversion [ 16 , 20 , 36 , 38 ]. Embryos in the genus Volvox also undergo a complete inversion, but a difference is that embryos are even spherical before inversion.…”

Section: Introductionmentioning

confidence: 99%

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Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

Höhn

Hallmann

2016

BMC Dev Biol

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Background: The multicellular volvocine alga Pleodorina is intermediate in organismal complexity between its unicellular relative, Chlamydomonas, and its multicellular relative, Volvox, which shows complete division of labor between different cell types. The volvocine green microalgae form a group of genera closely related to the genus Volvox within the order Volvocales (Chlorophyta). Embryos of multicellular volvocine algae consist of a cellular monolayer that, depending on the species, is either bowl-shaped or comprises a sphere. During embryogenesis, multicellular volvocine embryos turn their cellular monolayer right-side out to expose their flagella. This process is called 'inversion' and serves as simple model for epithelial folding in metazoa. While the development of spherical Volvox embryos has been the subject of detailed studies, the inversion process of bowl-shaped embryos is less well understood. Therefore, it has been unclear how the inversion of a sphere might have evolved from less complicated processes.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

Höhn

Hallmann

2016

BMC Dev Biol

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“…Inversion also exists in more basal volvocine relatives of Volvox [25,41], such as Pleodorina californica [42], Eudorina elegans [43-45], E. indica [46], Pandorina morum [47], Platydorina caudata [48] and Gonium pectorale [44,49,50], even if the process is less distinct in these species.…”

Section: Introductionmentioning

confidence: 99%

There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator

2011

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BackgroundEpithelial folding is a common morphogenetic process during the development of multicellular organisms. In metazoans, the biological and biomechanical processes that underlie such three-dimensional (3D) developmental events are usually complex and difficult to investigate. Spheroidal green algae of the genus Volvox are uniquely suited as model systems for studying the basic principles of epithelial folding. Volvox embryos begin life inside out and then must turn their spherical cell monolayer outside in to achieve their adult configuration; this process is called 'inversion.' There are two fundamentally different sequences of inversion processes in Volvocaceae: type A and type B. Type A inversion is well studied, but not much is known about type B inversion. How does the embryo of a typical type B inverter, V. globator, turn itself inside out?ResultsIn this study, we investigated the type B inversion of V. globator embryos and focused on the major movement patterns of the cellular monolayer, cell shape changes and changes in the localization of cytoplasmic bridges (CBs) connecting the cells. Isolated intact, sectioned and fragmented embryos were analyzed throughout the inversion process using light microscopy, confocal laser scanning microscopy, scanning electron microscopy and transmission electron microscopy techniques. We generated 3D models of the identified cell shapes, including the localizations of CBs. We show how concerted cell-shape changes and concerted changes in the position of cells relative to the CB system cause cell layer movements and turn the spherical cell monolayer inside out. The type B inversion of V. globator is compared to the type A inversion in V. carteri.ConclusionsConcerted, spatially and temporally coordinated changes in cellular shapes in conjunction with concerted migration of cells relative to the CB system are the causes of type B inversion in V. globator. Despite significant similarities between type A and type B inverters, differences exist in almost all details of the inversion process, suggesting analogous inversion processes that arose through parallel evolution. Based on our results and due to the cellular biomechanical implications of the involved tensile and compressive forces, we developed a global mechanistic scenario that predicts epithelial folding during embryonic inversion in V. globator.

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“…Gonium is the only genus in which inversion is “incomplete” meaning that a curved sheet of post-mitotic embryonic cells reverses its curvature so that the initially concave face where flagella will form becomes the convex face; but the post-inversion cell sheet never closes into a ball (Iida et al, 2013). In the larger-sized genera with complete inversion— Pandorina , Eudorina , and Pleodorina —embryos start out bowl-shaped and also reverse their curvature, but then undergo a process of closure where the free edges of the embryo join together to form an enclosed ball shape (Hallmann, 2006; Kikuchi, 1978; Marchant, 1977). Volvox embryos also undergo complete inversion as they start out sphere-shaped and are able to flip completely inside out to make an inverted sphere-shaped embryo.…”

Section: Inversion: Green Algal “Gastrulation”mentioning

confidence: 99%

Volvox: A simple algal model for embryogenesis, morphogenesis and cellular differentiation

Matt

Umen

2016

Developmental Biology

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Patterning of a multicellular body plan involves a coordinated set of developmental processes that includes cell division, morphogenesis, and cellular differentiation. These processes have been most intensively studied in animals and land plants; however, deep insight can also be gained by studying development in simpler multicellular organisms. The multicellular green alga Volvox carteri (Volvox) is an excellent model for the investigation of developmental mechanisms and their evolutionary origins. Volvox has a streamlined body plan that contains only a few thousand cells and two distinct cell types: reproductive germ cells and terminally differentiated somatic cells. Patterning of the Volvox body plan is achieved through a stereotyped developmental program that includes embryonic cleavage with asymmetric cell division, morphogenesis, and cell-type differentiation. In this review we provide an overview of how these three developmental processes give rise to the adult form in Volvox and how developmental mutants have provided insights into the mechanisms behind these events. We highlight the accessibility and tractability of Volvox and its relatives that provide a unique opportunity for studying development.

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Cellular differentiation in Pleodorina californica.

Cited by 13 publications

References 2 publications

Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator

Volvox: A simple algal model for embryogenesis, morphogenesis and cellular differentiation

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