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Cell-specific expression and individual function of prohormone convertase PC1/3 in Tribolium larval growth highlights major evolutionary changes between beetle and fly neuroendocrine systems
EvoDevo ( IF 4.1 ) Pub Date : 2021-06-29 , DOI: 10.1186/s13227-021-00179-w
Sonja Fritzsche 1 , Vera S Hunnekuhl 1
Affiliation  

The insect neuroendocrine system acts in the regulation of physiology, development and growth. Molecular evolution of this system hence has the potential to allow for major biological differences between insect groups. Two prohormone convertases, PC1/3 and PC2, are found in animals and both function in the processing of neuropeptide precursors in the vertebrate neurosecretory pathway. Whereas PC2-function is conserved between the fly Drosophila and vertebrates, ancestral PC1/3 was lost in the fly lineage and has not been functionally studied in any protostome. In order to understand its original functions and the changes accompanying the gene loss in the fly, we investigated PC1/3 and PC2 expression and function in the beetle Tribolium castaneum. We found that PC2 is broadly expressed in the nervous system, whereas surprisingly, PC1/3 expression is restricted to specific cell groups in the posterior brain and suboesophageal ganglion. Both proteases have parallel but non-redundant functions in adult beetles’ viability and fertility. Female infertility following RNAi is caused by a failure to deposit sufficient yolk to the developing oocytes. Larval RNAi against PC2 produced moulting defects where the larvae were not able to shed their old cuticle. This ecdysis phenotype was also observed in a small subset of PC1/3 knockdown larvae and was strongest in a double knockdown. Unexpectedly, most PC1/3-RNAi larvae showed strongly reduced growth, but went through larval moults despite minimal to zero weight gain. The cell type-specific expression of PC1/3 and its essential requirement for larval growth highlight the important role of this gene within the insect neuroendocrine system. Genomic conservation in most insect groups suggests that it has a comparable individual function in other insects as well, which has been replaced by alternative mechanisms in flies.

中文翻译:

细胞特异性表达和激素原转化酶的个别功能PC1 / 3幼虫和甲虫之间增长亮点主要进化变化飞神经内分泌系统

昆虫神经内分泌系统在生理、发育和生长的调节中起作用。因此,该系统的分子进化有可能允许昆虫群体之间的主要生物学差异。在动物中发现了两种激素原转化酶 PC1/3 和 PC2,它们都在脊椎动物神经分泌途径中的神经肽前体加工中起作用。PC2 功能在果蝇和脊椎动物之间是保守的,而祖先 PC1/3 在果蝇谱系中丢失,并且尚未在任何原生动物中进行功能研究。为了了解其原始功能以及伴随果蝇基因丢失的变化,我们研究了甲虫 Tribolium castaneum 中 PC1/3 和 PC2 的表达和功能。我们发现 PC2 在神经系统中广泛表达,而令人惊讶的是,PC1/3 表达仅限于后脑和食管下神经节中的特定细胞群。两种蛋白酶在成年甲虫的生存力和繁殖力方面具有平行但非冗余的功能。RNAi 后的女性不育是由于未能将足够的卵黄沉积到发育中的卵母细胞造成的。针对 PC2 的幼虫 RNAi 产生蜕皮缺陷,其中幼虫无法脱落旧角质层。这种蜕皮表型也在一小部分 PC1/3 敲低幼虫中观察到,并且在双重敲低中最强。出乎意料的是,大多数 PC1/3-RNAi 幼虫的生长速度明显下降,尽管体重增加极少甚至为零,但仍经历了幼虫换羽。PC1/3 的细胞类型特异性表达及其对幼虫生长的基本要求突出了该基因在昆虫神经内分泌系统中的重要作用。大多数昆虫群体的基因组保守表明它在其他昆虫中也具有类似的个体功能,在果蝇中已被替代机制所取代。
更新日期:2021-06-29
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