Dataset Information

Diaphanous gene mutation affects spiral cleavage and chirality in snails.

ABSTRACT: L-R (left and right) symmetry breaking during embryogenesis and the establishment of asymmetric body plan are key issues in developmental biology, but the onset including the handedness-determining gene locus still remains unknown. Using pure dextral (DD) and sinistral (dd) strains of the pond snail Lymnaea stagnalis as well as its F2 through to F10 backcrossed lines, the single handedness-determining-gene locus was mapped by genetic linkage analysis, BAC cloning and chromosome walking. We have identified the actin-related diaphanous gene Lsdia1 as the strongest candidate. Although the cDNA and derived amino acid sequences of the tandemly duplicated Lsdia1 and Lsdia2 genes are very similar, we could discriminate the two genes/proteins in our molecular biology experiments. The Lsdia1 gene of the sinistral strain carries a frameshift mutation that abrogates full-length LsDia1 protein expression. In the dextral strain, it is already translated prior to oviposition. Expression of Lsdia1 (only in the dextral strain) and Lsdia2 (in both chirality) decreases after the 1-cell stage, with no asymmetric localization throughout. The evolutionary relationships among body handedness, SD/SI (spiral deformation/spindle inclination) at the third cleavage, and expression of diaphanous proteins are discussed in comparison with three other pond snails (L. peregra, Physa acuta and Indoplanorbis exustus).

SUBMITTER: Kuroda R

PROVIDER: S-EPMC5052593 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Diaphanous gene mutation affects spiral cleavage and chirality in snails.

Kuroda Reiko R Fujikura Kohei K Abe Masanori M Hosoiri Yuji Y Asakawa Shuichi S Shimizu Miho M Umeda Shin S Ichikawa Futaba F Takahashi Hiromi H

Scientific reports 20161006

L-R (left and right) symmetry breaking during embryogenesis and the establishment of asymmetric body plan are key issues in developmental biology, but the onset including the handedness-determining gene locus still remains unknown. Using pure dextral (DD) and sinistral (dd) strains of the pond snail Lymnaea stagnalis as well as its F<sub>2</sub> through to F<sub>10</sub> backcrossed lines, the single handedness-determining-gene locus was mapped by genetic linkage analysis, BAC cloning and chromo ...[more]

PMID: 27708420

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Project description:Left-right asymmetry in snails is intriguing because individuals of opposite chirality are either unable to mate or can only mate with difficulty, so could be reproductively isolated from each other. We have therefore investigated chiral evolution in the Japanese land snail genus Euhadra to understand whether changes in chirality have promoted speciation. In particular, we aimed to understand the effect of the maternal inheritance of chirality on reproductive isolation and gene flow. We found that the mitochondrial DNA phylogeny of Euhadra is consistent with a single, relatively ancient evolution of sinistral species and suggests either recent "single-gene speciation" or gene flow between chiral morphs that are unable to mate. To clarify the conditions under which new chiral morphs might evolve and whether single-gene speciation can occur, we developed a mathematical model that is relevant to any maternal-effect gene. The model shows that reproductive character displacement can promote the evolution of new chiral morphs, tending to counteract the positive frequency-dependent selection that would otherwise drive the more common chiral morph to fixation. This therefore suggests a general mechanism as to how chiral variation arises in snails. In populations that contain both chiral morphs, two different situations are then possible. In the first, gene flow is substantial between morphs even without interchiral mating, because of the maternal inheritance of chirality. In the second, reproductive isolation is possible but unstable, and will also lead to gene flow if intrachiral matings occasionally produce offspring with the opposite chirality. Together, the results imply that speciation by chiral reversal is only meaningful in the context of a complex biogeographical process, and so must usually involve other factors. In order to understand the roles of reproductive character displacement and gene flow in the chiral evolution of Euhadra, it will be necessary to investigate populations in which both chiral morphs coexist.

Project description:BACKGROUND:During early development, patterns of cell division-embryonic cleavage-accompany the gradual restriction of blastomeres to specific cell fates. In Spiralia, which include annelids, mollusks, and flatworms, "spiral cleavage" produces a highly stereotypic, spiral-like arrangement of blastomeres and swimming trochophore-type larvae with rotational (spiral) symmetry. However, starting at larval stages, spiralian larvae acquire elements of bilateral symmetry, before they metamorphose into fully bilateral juveniles. How this spiral-to-bilateral transition occurs is not known and is especially puzzling for the early differentiating brain and head sensory organs, which emerge directly from the spiral cleavage pattern. Here we present the developmental cell lineage of the Platynereis larval episphere. RESULTS:Live-imaging recordings from the zygote to the mid-trochophore stage (~?30 hpf) of the larval episphere of the marine annelid Platynereis dumerilii reveal highly stereotypical development and an invariant cell lineage of early differentiating cell types. The larval brain and head sensory organs develop from 11 pairs of bilateral founders, each giving rise to identical clones on the right and left body sides. Relating the origin of each bilateral founder pair back to the spiral cleavage pattern, we uncover highly divergent origins: while some founder pairs originate from corresponding cells in the spiralian lineage on each body side, others originate from non-corresponding cells, and yet others derive from a single cell within one quadrant. Integrating lineage and gene expression data for several embryonic and larval stages, we find that the conserved head patterning genes otx and six3 are expressed in bilateral founders representing divergent lineage histories and giving rise to early differentiating cholinergic neurons and head sensory organs, respectively. CONCLUSIONS:We present the complete developmental cell lineage of the Platynereis larval episphere, and thus the first comprehensive account of the spiral-to-bilateral transition in a developing spiralian. The bilateral symmetry of the head emerges from pairs of bilateral founders, similar to the trunk; however, the head founders are more numerous and show striking left-right asymmetries in lineage behavior that we relate to differential gene expression.

Dataset Information

Diaphanous gene mutation affects spiral cleavage and chirality in snails.

Publications

Diaphanous gene mutation affects spiral cleavage and chirality in snails.

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