Cell-cell interactions determine the dorsoventral axis in embryos of an equally cleaving opisthobranch mollusc

Boring, Landin

doi:10.1016/0012-1606(89)90145-0

Cited by 51 publications

(19 citation statements)

References 37 publications

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“…He commented, “it appears that the 4D macromere contributes nutriment to the developing larva, but lacks any essential morphogenetic value.” Similar results were obtained for the gastropods C. fornicata (Henry et al. ), Lymnaea stagnalis ( Linnaeus 1758) (Martindale ), and Haminoea japonica Pilsbry 1895 (Boring ; this species was formerly known as H. callidegenita , as discussed by Gosliner & Behrens ), and for a scaphopod ( Dentalium sp. : Cather & Verdonk ).…”

supporting

confidence: 76%

“…). Further, in the several molluscs in which relevant macromere deletion experiments have been carried out (with the aim of understanding the mechanism of dorsal‐ventral axis establishment: Clement ; Cather & Verdonk ; Martindale ; Boring ; Henry et al. ), deletion seems to have little effect on morphogenesis, resulting in larvae or juveniles that are morphologically normal but smaller than controls.…”

Section: Discussionmentioning

confidence: 99%

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Effects of maternal investment on larvae and juveniles of the annelidCapitella teletadetermined by experimental reduction of embryo energy content

Pernet

Amiel

Seaver

2012

Invertebrate Biology

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Experimental manipulations of the energy content of marine invertebrate embryos have been useful in testing key assumptions of life history theory, especially those concerning relationships between egg size, length of the planktonic period, and juvenile size and quality. However, methods for such “allometric engineering” experiments have been available for only a limited set of taxa (those with regulative early development, e.g., cnidarians and echinoderms). Here, we describe a method for the reduction of embryo energy content in the spirally cleaving embryos of a marine annelid, Capitella teleta, by targeted deletion of endodermal precursor cells. Embryos of C. teleta in which up to three cells (the macromeres 3A, 3B, and 3C) were deleted formed morphologically normal lecithotrophic larvae that were much smaller than larvae developing from control embryos. Experimental larvae metamorphosed at high rates, forming juveniles that were smaller than control juveniles. Juveniles derived from treated embryos had functional midguts, ingested and digested food, and grew into sexually mature adults. These results are consistent with those from previous allometric engineering studies of echinoid echinoderms, which suggest that in facultatively planktotrophic or lecithotrophic species, little maternally derived energy is used for construction of the larval body; instead, the majority is allocated to the formation of a large, high‐quality juvenile. Cleavage programs are highly conserved among divergent spiralian taxa (e.g., molluscs, nemerteans, and platyhelminths), so this method will likely be applicable to a diverse set of embryos. Similar experiments carried out in these diverse taxa will be extremely useful for evaluating inferences on relationships between egg size, length of the planktonic period, and juvenile size and quality previously based only on experiments on echinoid echinoderms.

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supporting

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Effects of maternal investment on larvae and juveniles of the annelidCapitella teletadetermined by experimental reduction of embryo energy content

Pernet

Amiel

Seaver

2012

Invertebrate Biology

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“…This happens sometime during the 24-63 cell stages and has been described for the gastropods Patella and Haliotis as well as the polyplacophoran Acanthochiton (van den Biggelaar and Guerrier 1979 ; Arnolds et al 1983 ;Boring 1989 ; van den Biggelaar 1996 ; see also Wanninger et al 2008 ;Nielsen 2012 ). In experimental studies, inhibition of 3D induction has resulted in nonbilateral and largely disorganized embryos similar to ones raised after polar lobe deletion (van den Biggelaar 1977 ;Martindale et al 1985 ;Martindale 1986 ;Kühtreiber et al 1988 ;Damen and Dictus 1996 ;Lambert and Nagy 2003 ).…”

Section: Cell Lineage and The 4d Cellmentioning

confidence: 84%

Mollusca

Wanninger

Wollesen

2015

Evolutionary Developmental Biology of Invertebrates 2

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“…In equal-cleaving spiralians, any quadrant may become the D quadrant (van den Biggelaar and Guerrier, 1979;Arnolds, et al, 1983;Martindale et al, 1985;Kuhtreiber et al, 1988;Boring, 1989;van den Biggelaar, 1996;Henry, 2002;Henry et al, 2006). While there is a bias favoring the two vegetal cross-furrow macromeres due to their central location beneath the first quartet derivatives, only a single quadrant ultimately becomes the D quadrant Henry, 2002).…”

Section: Comparative Mechanisms Of Cell Fate and Axis Determination: mentioning

confidence: 99%

“…In equal-cleaving embryos without polar lobes the dorsal (D) cell quadrant is determined later during development by virtue of cell-cell inductive interactions between derivatives of the first quartet micromeres (1a 1 - 1d 1 ) and one of the vegetal macromeres (presumptive 3D macromere) after the birth of the third quartet (van den Biggelaar and Guerrier, 1979;Arnolds et al, 1983;Martindale et al, 1985;Kuhtreiber et al, 1988;Boring, 1989;van den Biggelaar, 1996;Henry, 2002).…”

Section: Comparative Mechanisms Of Cell Fate and Axis Determination: mentioning

confidence: 99%

The Slipper Snail, Crepidula: An Emerging Lophotrochozoan Model System

Henry

Collin

Perry

2010

The Biological Bulletin

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Abstract. Recent developmental and genomic research focused on "slipper snails" in the genus Crepidula has positioned Crepidula fornicata as a de facto model system for lophotrochozoan development. Here we review recent developments, as well as earlier reports demonstrating the widespread use of this system in studies of development and life history. Recent studies have resulted in a well-resolved fate map of embryonic cell lineage, documented mechanisms for axis determination and D quadrant specification, preliminary gene expression patterns, and the successful application of loss-and gain-of-function assays. The recent development of expressed sequence tags and preliminary genomics work will promote the use of this system, particularly in the area of developmental biology. A wealth of comparative information on phylogenetic relationships, variation in mode of development within the family, and numerous studies on larval biology and metamorphosis, primarily in Crepidula fornicata, make these snails a powerful tool for studies of the evolution of the mechanisms of development in the Mollusca and Lophotrochozoa. By bringing a review of the current state of knowledge of Crepidula life histories and development together with some detailed experimental methods, we hope to encourage further use of this system in various fields of investigation.

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Cell-cell interactions determine the dorsoventral axis in embryos of an equally cleaving opisthobranch mollusc

Cited by 51 publications

References 37 publications

Effects of maternal investment on larvae and juveniles of the annelidCapitella teletadetermined by experimental reduction of embryo energy content

Effects of maternal investment on larvae and juveniles of the annelidCapitella teletadetermined by experimental reduction of embryo energy content

Mollusca

The Slipper Snail, Crepidula: An Emerging Lophotrochozoan Model System

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