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Heterochirality results from reduction of maternal diaph expression in a terrestrial pulmonate snail
Zoological Letters ( IF 2.7 ) Pub Date : 2019-01-10 , DOI: 10.1186/s40851-018-0120-0
Takeshi Noda 1 , Noriyuki Satoh 2 , Takahiro Asami 1
Affiliation  

Spiral cleavage is a feature of non-ecdysozoan protostomes, in which left-right reversal frequently evolved in gastropod molluscs. In pulmonate gastropods, maternal molecules are responsible for chirality patterning, on which the polarities of visceral and coiling asymmetries depend. In the pond snail, Lymnaea stagnalis (the clade Hygrophila), a frame-shift mutation of one of tandem-duplicated, diaphanous-related formin genes (diaph) resulted in incomplete reversal from dextral to sinistral cleavage. Is this mechanism of chirality regulation common to, or shared with other pulmonates? To answer this question, we examined genes involved in chirality patterning in the land snail, Bradybaena similaris which belongs to the clade Stylommatophora. Both dextral and sinistral siblings develop from progeny of a racemic mutant of B. similaris. Differences in maternal mRNAs between the two strains were searched by transcriptome analyses. We found fifty maternal transcripts that exhibited less expression in early embryos of the mutant strain. The most conspicuous was a homolog of diaph. The diaph gene was duplicated in the stylommatophoran ancestor (diaph-a and diaph-b), as in the case of the ancestor of Lymnaea (Lsdiaph1 and Lsdiaph2). The quantity of maternal diaph-b mRNA was drastically reduced in early embryos of the racemic mutant compared to wild-type, while diaph-a expression was at nearly the same level in both strains. Unlike the case of Lsdiaph2, which is frame-shifted to produce truncated peptides in the mutant of L. stagnalis, however, Bsdiaph-b mRNA in the mutant strain is not frame-shifted and most probably produces normal Diaph-b protein. These results suggest the presence of regulatory mechanisms of gene expression for chirality patterning in pulmonate gastropods, although genomic analyses are required for confirmation. Heterochirality resulting from the loss of polarity control in spiral cleavage does not require mutation of the diaph gene in B. similaris. The determination of left-right polarity instead depends on the expression of this diaph gene, which is duplicated in stylommatophoran Bradybaena, as well as in hygrophilan Lymnaea. Our results provide an avenue to identifying a regulatory mechanism that controls the direction of spiral cleavage in gastropods.

中文翻译:

异手性是由陆生肺蜗牛母体横膈膜表达减少引起的

螺旋分裂是非蜕皮动物原生动物的一个特征,其中左右反转经常在腹足类软体动物中进化。在有肺腹足动物中,母体分子负责手性模式,内脏和盘绕不对称的极性依赖于此。在池塘蜗牛,Lymnaea stagnalis(嗜水进化枝)中,一个串联重复的透明相关的formin基因(diaph)的移码突变导致从右旋到左旋卵裂的不完全逆转。这种手性调节机制是常见的,还是与其他肺动脉共享的?为了回答这个问题,我们检查了与陆地蜗牛手性模式有关的基因,Bradybaenasimilaris 属于进化枝 Stylommatophora。右旋和左旋兄弟姐妹都是从 B.similaris 的外消旋突变体的后代发育而来的。通过转录组分析搜索两种菌株之间母体mRNA的差异。我们发现五十个母体转录本在突变株的早期胚胎中表现出较少的表达。最显眼的是横膈膜的同系物。diaph 基因在 stylommatophoran 的祖先(diaph-a 和 diaph-b)中复制,就像 Lymnaea 的祖先(Lsdiaph1 和 Lsdiaph2)一样。与野生型相比,外消旋突变体早期胚胎中母体diaph-b mRNA的数量急剧减少,而两种菌株的diaph-a表达水平几乎相同。然而,与 Lsdiaph2 的情况不同,Lsdiaph2 在 L. stagnalis 的突变体中移码以产生截短的肽,然而,突变菌株中的 Bsdiaph-b mRNA 没有移码,并且很可能产生正常的 Diaph-b 蛋白。这些结果表明存在肺腹足动物手性模式的基因表达调控机制,尽管需要基因组分析来确认。由于螺旋切割中极性控制丧失而导致的异手性不需要在 B.similaris 中对横断面基因进行突变。相反,左右极性的确定取决于这种横膈膜基因的表达,该基因在 stylomatophoran Bradybaena 和 hygrophilan Lymnaea 中重复。我们的研究结果为确定控制腹足动物螺旋劈裂方向的调节机制提供了一条途径。由于螺旋切割中极性控制丧失而导致的异手性不需要在 B.similaris 中对横断面基因进行突变。相反,左右极性的确定取决于这种横膈膜基因的表达,该基因在 stylomatophoran Bradybaena 和 hygrophilan Lymnaea 中重复。我们的研究结果为确定控制腹足动物螺旋劈裂方向的调节机制提供了一条途径。由于螺旋切割中极性控制丧失而导致的异手性不需要在 B.similaris 中对横断面基因进行突变。相反,左右极性的确定取决于这种横膈膜基因的表达,该基因在 stylomatophoran Bradybaena 和 hygrophilan Lymnaea 中重复。我们的研究结果为确定控制腹足动物螺旋劈裂方向的调节机制提供了一条途径。
更新日期:2020-04-22
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