Left-right asymmetric expression of dpp in the mantle of gastropods correlates with asymmetric shell coiling

Shimizu, Keisuke; Iijima, Mayumi; Setiamarga, Davin H. E.; Sarashina, Isao; Kudoh, Tetsuhiro; Asami, Takahiro; Gittenberger, Edi; Endo, Kazuhiko

doi:10.1186/2041-9139-4-15

Cited by 28 publications

(15 citation statements)

References 17 publications

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“…The subsequent direction of shell coiling in later development seen in B. glabrata and L. stagnalis morphs also correlated with sidedness of gene expression. It has also been shown that asymmetric growth and torsion in larval snails is driven by TGF-b signaling (Kurita and Wada, 2011), with the TGF-b superfamily ligand Dpp (BMP2/4 or Decapentaplegic) suggested to integrate asymmetric cues in postembryonic shell morphogenesis through a gradient of Dpp in the shell gland (Shimizu et al, 2011(Shimizu et al, , 2013. Despite these advances, much remains unknown, with most studies only considering gastropod molluscs.…”

Section: Asymmetry In the Lophotrochozoamentioning

confidence: 99%

Right across the tree of life: The evolution of left–right asymmetry in the Bilateria

Namigai

Kenny

Shimeld

2014

Genesis

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Directional left/right (LR) asymmetries, in which there are consistent, heritable differences in morphology between the left and right sides of bilaterally symmetrical organisms, are found in animals across the Bilateria. For many years, we have lacked evidence for shared mechanisms underlying their development. This led to the supposition that the mechanisms driving establishment of LR asymmetries, and consequently the asymmetries themselves, had evolved separately in the three major Superphyla that constitute the Bilateria. The recent discovery that the transforming growth factor-beta (TGF-B) ligand Nodal plays a role in the regulation of LR asymmetry in both Deuterostomia and Lophotrochozoa has reignited debate in this field, as it suggests that at least this aspect of the development of the LR axis is conserved. In this review, we discuss evidence for shared mechanisms of LR asymmetry establishment across the bilaterian tree of life and consider how these mechanisms might have diverged across the Metazoa over the last 500 million years or so of evolution. As well as the likelihood that Nodal is an ancestral mechanism for regulating LR asymmetry, we reemphasize cytoskeletal architecture as a potential shared mechanism underlying symmetry breaking. However, convergent evolution remains a distinct possibility and study of a wider diversity of species will be needed to distinguish between conserved and lineage-specific mechanisms. genesis 52:458-470,

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Section: Asymmetry In the Lophotrochozoamentioning

confidence: 99%

Right across the tree of life: The evolution of left–right asymmetry in the Bilateria

Namigai

Kenny

Shimeld

2014

Genesis

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“…Some developmental regulatory genes are expressed in the mantle epithelium that generates the shell (11)(12)(13)(14)(15)(16). The growth factor dpp/BMP2-4 has been implicated in mantle proliferation (17)(18)(19)(20)(21). In the bivalve Pinctada fucata, a gradient of proliferation perpendicular to the mantle edge has been reported, with generally higher proliferation in interior parts of the mantle and lower rates in zones near the outer edges (22).…”

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confidence: 99%

Growth and morphogenesis of the gastropod shell

Johnson

Fogel

Lambert

2019

Proc. Natl. Acad. Sci. U.S.A.

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Gastropod shell morphologies are famously diverse but generally share a common geometry, the logarithmic coil. Variations on this morphology have been modeled mathematically and computationally but the developmental biology of shell morphogenesis remains poorly understood. Here we characterize the organization and growth patterns of the shell-secreting epithelium of the larval shell of the basket whelkTritia(also known asIlyanassa). Despite the larval shell’s relative simplicity, we find a surprisingly complex organization of the shell margin in terms of rows and zones of cells. We examined cell division patterns with EdU incorporation assays and found two growth zones within the shell margin. In the more anterior aperture growth zone, we find that inferred division angles are biased to lie parallel to the shell edge, and these divisions occur more on the margin’s left side. In the more posterior mantle epithelium growth zone, inferred divisions are significantly biased to the right, relative to the anterior–posterior axis. These growth zones, and the left–right asymmetries in cleavage patterns they display, can explain the major modes of shell morphogenesis at the level of cellular behavior. In a gastropod with a different coiling geometry,Planorbellasp., we find similar shell margin organization and growth zones asTritia, but different left–right asymmetries than we observed in the helically coiled shell ofTritia. These results indicate that differential growth patterns in the mantle edge epithelium contribute to shell shape in gastropod shells and identify cellular mechanisms that may vary to generate shell diversity in evolution.

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“…This is in stark contrast to the situation in L. stagnalis. Furthermore, while other research groups have previously reported WMISH expression patterns for several genes in L. stagnalis larvae (see 22,28,29 ) the method that we describe here yields patterns of significantly higher spatial resolution. Finally, we have observed significant inter-batch variation in the activity of the Proteinase-K from our supplier.…”

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confidence: 78%

A Whole Mount <em>In Situ</em> Hybridization Method for the Gastropod Mollusc <em>Lymnaea stagnalis</em>

Herlitze

Hohagen

2016

JoVE

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Whole mount in situ hybridization (WMISH) is a technique that allows for the spatial resolution of nucleic acid molecules (often mRNAs) within a 'whole mount' tissue preparation, or developmental stage (such as an embryo or larva) of interest. WMISH is extremely powerful because it can significantly contribute to the functional characterization of complex metazoan genomes, a challenge that is becoming more of a bottleneck with the deluge of next generation sequence data. Despite the conceptual simplicity of the technique much time is often needed to optimize the various parameters inherent to WMISH experiments for novel model systems; subtle differences in the cellular and biochemical properties between tissue types and developmental stages mean that a single WMISH method may not be appropriate for all situations. We have developed a set of WMISH methods for the re-emerging gastropod model Lymnaea stagnalis that generate consistent and clear WMISH signals for a range of genes, and across all developmental stages. These methods include the assignment of larvae of unknown chronological age to an ontogenetic window, the efficient removal of embryos and larvae from their egg capsules, the application of an appropriate Proteinase-K treatment for each ontogenetic window, and hybridization, post-hybridization and immunodetection steps. These methods provide a foundation from which the resulting signal for a given RNA transcript can be further refined with probe specific adjustments (primarily probe concentration and hybridization temperature).

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Left-right asymmetric expression of dpp in the mantle of gastropods correlates with asymmetric shell coiling

Cited by 28 publications

References 17 publications

Right across the tree of life: The evolution of left–right asymmetry in the Bilateria

Right across the tree of life: The evolution of left–right asymmetry in the Bilateria

Growth and morphogenesis of the gastropod shell

A Whole Mount <em>In Situ</em> Hybridization Method for the Gastropod Mollusc <em>Lymnaea stagnalis</em>

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