Embryogenesis and cell positioning in<i>Platydorina caudata</i>(Volvocaceae, Chlorophyta)

Iida, Hitoshi; Nishii, Ichiro; Inouye, Isao

doi:10.2216/10-80.1

Cited by 11 publications

(11 citation statements)

References 30 publications

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“…Similar vesicles have been observed in asexual reproductive cells of V. carteri [ 4 ]. Elongated teardrop-shaped cells also occur in inverting embryos of Platydorina caudata [ 23 ]; however, it should be noted that in the specified publication the cells are misleadingly referred to as spindle-shaped, even though the corresponding cells clearly have rounded apical cell halves.…”

Section: Discussionmentioning

confidence: 99%

“…In Platydorina caudata , the fully cleaved, pre-inversion embryos comprise a slightly concave plate of 16 cells with conical apical cell poles [ 23 ]. The cells are connected with each other by CBs that are localized close to their cell equators.…”

Section: Discussionmentioning

confidence: 99%

“…In the smaller multicellular relatives of Pleodorina , which consist of only 8 to 32 cells, all cells have reproductive capabilities. The adults of those multicellular volvocine genera with 8 to 32 cells are either organized as almost flat or bowl shaped cell sheets ( Platydorina [ 22 , 23 ] , Gonium [ 18 , 24 – 27 ]) or as small spheroids ( Pandorina [ 28 ] , Volvulina [ 29 , 30 ] , Eudorina [ 16 , 31 ] , Yamagishiella [ 21 ]) (Fig. 1 , Additional file 1 ).…”

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%

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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: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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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Cleavage, incomplete inversion, and cytoplasmic bridges in Gonium pectorale (Volvocales, Chlorophyta)

2013

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Multicellularity arose several times in evolution of eukaryotes. The volvocine algae have full range of colonial organization from unicellular to colonies, and thus these algae are well-known models for examining the evolution and mechanisms of multicellularity. Gonium pectorale is a multicellular species of Volvocales and is thought to be one of the first small colonial organisms among the volvocine algae. In these algae, a cytoplasmic bridge is one of the key traits that arose during the evolution of multicellularity. Here, we observed the inversion process and the cytoplasmic bridges in G. pectorale using time-lapse, fluorescence, and electron microscopy. The cytoplasmic bridges were located in the middle region of the cell in 2-, 4-, 8-, and 16-celled stages and in inversion stages. However, there were no cytoplasmic bridges in the mature adult stage. Cytoplasmic bridges and cortical microtubules in G. pectorale suggest that a mechanism of kinesin-microtubule machinery similar to that in other volvocine algae is responsible for inversion in this species.

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Embryogenesis and cell positioning inPlatydorina caudata(Volvocaceae, Chlorophyta)

Cited by 11 publications

References 30 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

Cleavage, incomplete inversion, and cytoplasmic bridges in Gonium pectorale (Volvocales, Chlorophyta)

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