Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies.

Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies.
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DOI:
10.1186/s12915-023-01602-5
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发表时间:
2023-05-11
期刊:
影响因子:
5.4
通讯作者:
Kronforst, Marcus R.
Kronforst, Marcus R.
中科院分区:
生物学2区
文献类型:
--
作者:
Bayala, Erick X.;Cisneros, Isabella;Massardo, Darli;VanKuren, Nicholas W.;Kronforst, Marcus R.

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基因复制事件对于新基因功能的进化至关重要。无阿里斯塔勒斯是不同发育过程的主要调节器。它因其在动物附肢发育过程中的作用而最为人们所知。然而,最近已经描述了该基因及其复制品的其他不同的生物学功能。蝴蝶和飞蛾有两个无芒基因的拷贝,无芒1(al 1)和无芒2(al 2),这是基因复制的结果。以前在Heliconius的工作表明,这两个副本似乎都具有与翅膀颜色图案相关的新功能。在这里,我们扩大我们的知识与A11跨胚胎发生和翅膀色素沉着的祖先和新的功能相关的表达谱。此外,我们表征铝2的表达,在同一物种内的基因拷贝之间提供了一个比较框架,使我们能够了解基因复制后的新功能的起源。我们的工作表明,铝1和铝2的表达与祖先的感觉附属器(腿,嘴,脊柱和眼睛)在胚胎中的发育功能。有趣的是,Al 1在胚胎发生早期表现出较高的表达,而Al 2表达的最高水平转移到胚胎发育的后期阶段。此外,Al 1定位出现在核外,而Al 2在早期与核紧密共定位,然后在发育后期也扩展到核外。细胞表达的铝1和铝2蛹翅膀是大致一致的模式在胚胎发育过程中观察到的。我们还描述了,第一次,铝1本地化似乎与区域的前/后伸长的身体在胚胎生长过程中,展示了一个可能的新功能相关的Aristaless'以前描述的附件扩展的作用。总的来说,我们的数据表明,虽然这两个基因拷贝在胚胎发生和翅膀色素沉着中发挥作用,但重复的基因在这些功能中在时间和机制上有所不同。我们的研究有助于阐明与基因重复事件后发育功能相关的亚功能化和基因表达进化背后的原则。在线版本包含补充材料,可通过10.1186/s12915-023-01602-5获得。
Gene duplication events are critical for the evolution of new gene functions. Aristaless is a major regulator of distinct developmental processes. It is most known for its role during appendage development across animals. However, more recently other distinct biological functions have been described for this gene and its duplicates. Butterflies and moths have two copies of aristaless, aristaless1 (al1) and aristaless2 (al2), as a result of a gene duplication event. Previous work in Heliconius has shown that both copies appear to have novel functions related to wing color patterning. Here we expand our knowledge of the expression profiles associated with both ancestral and novel functions of Al1 across embryogenesis and wing pigmentation. Furthermore, we characterize Al2 expression, providing a comparative framework between gene copies within the same species, allowing us to understand the origin of new functions following gene duplication. Our work shows that the expression of both Al1 and Al2 is associated with the ancestral function of sensory appendage (leg, mouth, spines, and eyes) development in embryos. Interestingly, Al1 exhibits higher expression earlier in embryogenesis while the highest levels of Al2 expression are shifted to later stages of embryonic development. Furthermore, Al1 localization appears extranuclear while Al2 co-localizes tightly with nuclei earlier, and then also expands outside the nucleus later in development. Cellular expression of Al1 and Al2 in pupal wings is broadly consistent with patterns observed during embryogenesis. We also describe, for the first time, how Al1 localization appears to correlate with zones of anterior/posterior elongation of the body during embryonic growth, showcasing a possible new function related to Aristaless’ previously described role in appendage extension. Overall, our data suggest that while both gene copies play a role in embryogenesis and wing pigmentation, the duplicates have diverged temporally and mechanistically across those functions. Our study helps clarify principles behind sub-functionalization and gene expression evolution associated with developmental functions following gene duplication events. The online version contains supplementary material available at 10.1186/s12915-023-01602-5.
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