Development of the house secreting epithelium, a major innovation of tunicate larvaceans, involves multiple homeodomain transcription factors

Mikhaleva, Yana; Skinnes, Ragnhild; Sumić, Sara; Thompson, Eric M.; Chourrout, Daniel

doi:10.1016/j.ydbio.2018.09.006

Cited by 10 publications

(21 citation statements)

References 39 publications

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“…The OE cell specification may occur depending on the cell position around hatching or later stages after the OE precursor cells are spatially arranged bilaterally (Kishi et al., 2017). In accordance with this notion, several homeobox transcription factor genes show distinct expression in hatched larva before OE specification (Mikhaeva et al., 2018). RNAi‐mediated knockdown of propA or propB caused a reduction of some dorsal midline cells, and abrogated the region‐specific oikosin41 expression (Mikhaeva et al., 2018).…”

Section: Imagingmentioning

confidence: 71%

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Developmental biology of the larvaceanOikopleura dioica: Genome resources, functional screening, and imaging

Onuma

Nishida

2021

Dev Growth Differ

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The larvacean Oikopleura dioica is a cosmopolitan planktonic chordate and is closely related to vertebrates. It is characterized by a tadpole‐shaped morphology with notochord flanked by muscle in the tail and brain on the dorsal side, a short life cycle of five days, a compact genome of approximately 56 Mb, a simple and transparent body with a small number of cells (~4000 in functional juveniles), invariant embryonic cell lineages, and fast development that ensures complete morphogenesis and organ formation 10 h after fertilization. With these features, this marine chordate is a promising and advantageous animal model in which genetic manipulation is feasible. In this review, we introduce relevant resources and modern techniques that have been developed: (1) Genome and transcriptomes. Oikopleura dioica has the smallest genome among non‐parasitic metazoans. Its genome databases have been generated using three geographically distant O. dioica populations, and several intra‐species sequence differences are becoming evident; (2) Functional genetic knockdown techniques. Comprehensive screening of genes is feasible using ovarian microinjection and double‐strand DNA‐induced gene knockdown; and (3) Live imaging of embryos and larvae. Application of these techniques has uncovered novel aspects of development, including meiotic cell arrest, left–right patterning, epidermal cell patterning, and mouth formation involving the connection of ectoderm and endoderm sheets. Oikopleura dioca has become very useful for developmental and evolutionary studies in chordates.

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Section: Imagingmentioning

confidence: 71%

“…In accordance with this notion, several homeobox transcription factor genes show distinct expression in hatched larva before OE specification (Mikhaeva et al., 2018). RNAi‐mediated knockdown of propA or propB caused a reduction of some dorsal midline cells, and abrogated the region‐specific oikosin41 expression (Mikhaeva et al., 2018).…”

Section: Imagingmentioning

confidence: 71%

Developmental biology of the larvaceanOikopleura dioica: Genome resources, functional screening, and imaging

Onuma

Nishida

2021

Dev Growth Differ

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“…However, the authors showed that the regional specific expression of the oikosins in the oikoplastic epithelium corresponds to spatially restricted presence of the corresponding oikosins in the house. Mikhaleva et al (2018) showed that the expression of the approximately 80 known variants of oikosin genes in O . dioica is developmentally controlled by hox genes.…”

Section: Discussionmentioning

confidence: 99%

The filter‐house of the larvaceanOikopleura dioica. A complex extracellular architecture: From fiber production to rudimentary state to inflated house

Razghandi

Janßen

et al. 2021

Journal of Morphology

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While cellulose is the most abundant macromolecule in the biosphere, most animals are unable to produce cellulose with the exception of tunicates. Some tunicates have evolved the ability to secrete a complex house containing cellulosic fibers, yet little is known about the early stages of the house building process.Here, we investigate the rudimentary house of Oikopleura dioica for the first time using complementary light and electron microscopic techniques. In addition, we digitally modeled the arrangement of chambers, nets, and filters of the functional, expanded house in three dimensions based on life-video-imaging. Combining 3Dreconstructions based on serial histological semithin-sections, confocal laser scanning microscopy, transmission electron microscopy, scanning electron microscopy (SEM), and focused ion beam (FIB)-SEM, we were able to elucidate the arrangement of structural components, including cellulosic fibers, of the rudimentary house with a focus on the food concentration filter. We developed a model for the arrangement of folded structures in the house rudiment and show it is a precisely preformed structure with identifiable components intricately correlated with specific cells. Moreover, we demonstrate that structural details of the apical surfaces of Nasse cells provide the exact locations and shapes to produce the fibers of the house and interact among each other, with Giant Fol cells, and with the fibers to arrange them in the precise positions necessary for expansion of the house rudiment into the functional state. The presented data and hypotheses advance our knowledge about the interrelation of structure and function on different biological levels and prompt investigations into this astonishing biological object.

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“…Finally, the loss of muscles to propel fluid inside the organism could be considered the result of regressive evolution during the transition from a sessile filter-feeding ascidian-like strategy, in which contraction of siphon muscles is responsible for water current, to a pelagic filter-feeding strategy based on the innovation of the appendicularian house, in which water circulation is mostly propelled by tail beating 68 . Considering that in addition of tail beating, water circulation is also propelled by fined tuned movement of the cilia in the gills that can efficiently reverse the direction of the water flow, inwards during feeding or outwards during the inflation of the house, it is also plausible to think that instead of being a process of regressive evolution, the loss of In conclusion, our results support an evolutionary adaptive scenario in which the deconstruction of cardiopharyngeal GRN could have contributed to the loss of features that characterize ascidianlike sessile lifestyle, and the acquisition of novel features that enabled its transition to a pelagic free-living active style connected to the innovation of the house (Fig.…”

Section: Evolution Of Pelagic Appendicularians From a Sessile Ascidiamentioning

confidence: 99%

Cardiopharyngeal deconstruction and ancestral tunicate sessility

Ferrández-Roldán

Fabrega-Torrus

Sánchez-Serna

et al. 2021

Preprint

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A key problem in understanding chordate evolution has been the origin of sessility of ascidians, and whether the appendicularian free-living style represents a primitive or derived condition of tunicates. To address this problem, we performed comprehensive developmental and genomic comparative analyses of the cardiopharyngeal gene regulatory network (GRN) between appendicularians and ascidians. Our results reveal that the cardiopharyngeal GRN has suffered a process of evolutionary deconstruction with massive ancestral losses of genes (Mesp, Ets1/2, Gata4/5/6, Mek1/2, Tbx1/10, and RA- and FGF-signaling related genes) and subfunctions (e.g. FoxF, Islet, Ebf, Mrf, Dach and Bmp signaling). These losses have led to the deconstruction of two modules of the cardiopharyngeal GRN that in ascidians are related to early and late multipotent state cells involved in lineage fate determination towards first and secondary heart fields, and siphon muscle. Our results allow us to propose an evolutionary scenario, in which the evolutionary deconstruction of the cardiopharyngeal GRN has had an adaptive impact on the acceleration of the developmental cardiac program, the redesign of the cardiac architecture into an open-wide laminar structure, and the loss of pharyngeal muscle. Our findings, therefore, provide evidence supporting that the ancestral tunicate had a sessile ascidian-like lifestyle, and points to the deconstruction of the cardiopharyngeal GRN in appendicularians as a key event that facilitated the evolution of their pelagic free-living style connected to the innovation of the house.

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Development of the house secreting epithelium, a major innovation of tunicate larvaceans, involves multiple homeodomain transcription factors

Cited by 10 publications

References 39 publications

Developmental biology of the larvaceanOikopleura dioica: Genome resources, functional screening, and imaging

Developmental biology of the larvaceanOikopleura dioica: Genome resources, functional screening, and imaging

The filter‐house of the larvaceanOikopleura dioica. A complex extracellular architecture: From fiber production to rudimentary state to inflated house

Cardiopharyngeal deconstruction and ancestral tunicate sessility

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