The family of amphioxus chitin synthases offers insight into the evolution of chitin formation in chordates

The family of amphioxus chitin synthases offers insight into the evolution of chitin formation in chordates
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文昌鱼几丁质合酶家族提供了对脊索动物几丁质形成进化的深入了解

DOI:
10.1016/j.ympev.2019.106691
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发表时间:
2020
影响因子:
4.1
通讯作者:
Shengfeng Huang
Shengfeng Huang
中科院分区:
生物学1区
文献类型:
--
作者:
Yi Shi;Zhaoyu Fan;Guang Li;Lei Zhang;Zirui Yue;Xinyu Yan;Anlong Xu;Shengfeng Huang

文献摘要

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几丁质是真菌和低等后生动物中非常重要且广泛使用的生物聚合物,但在哺乳动物中却神秘消失。最近的研究表明,至少低等脊椎动物具有几丁质合酶(CS)并利用它们来合成内源性几丁质。因此,文昌鱼是一种基础脊索动物,对于理解 CS 的进化至关重要,因为它占据了从无脊椎动物到脊椎动物的过渡位置,并被认为是脊索动物祖先的良好代表。在这里,通过利用多个基因组组装、高深度 RNA-seq 数据和同线性关系,我们确定了每个文昌鱼物种的 11-12 个 CS 基因。它代表了迄今为止在真核生物中发现的最大的CS基因库。相比之下,大多数后生动物都有一个或两个 CS。文昌鱼是唯一同时拥有非常古老的 I 型 CS 家族和分布更广泛的 II 型 CS 家族的脊索动物。具体来说,文昌鱼只有一个II型CS,但有10-11个I型CS,这意味着文昌鱼是唯一一个拥有大大扩展的I型CS家族的后生动物。进一步的分析表明,脊索动物祖先至少有一个 II 型 CS 和一个扩展的 I 型 CS 家族。我们推测:这些古老的CS大部分保留在文昌鱼中;但整个 I 型 CS 家族在尾索动物和脊椎动物中消失了;随后,II 型 CS 在脊椎动物中复制成两个谱系,然后随机丢失,直到所有 II 型 CS 最终在鸟类和哺乳动物中消失。最后,我们的表达谱和初步基因敲除分析表明文昌鱼CSs在不同组织和器官中可能具有高度多样化但轻度重叠的功能。总而言之,这些发现不仅为脊索动物CSs的进化提供了见解,也为脊索动物CSs的进一步功能研究奠定了基础。毕竟,我们的脊索动物祖先需要如此多的同工酶来形成几丁质,这很神秘。
Chitin is a very important and widely-used biopolymer in fungi and lower metazoans, but mysteriously disappears in mammals. Recent studies reveal that at least lower vertebrates have chitin synthases (CS) and use them to synthesize endogenous chitin. Amphioxus, a basal chordate, therefore becomes critical to understand the evolution of CS, as it occupies the transitional position from invertebrates to vertebrates, and is considered as a good proxy to the chordate ancestor.Here, by exploiting multiple genome assemblies, high-depth RNA-seq data and synteny relations, we identify 11–12 CS genes for each amphioxus species. It represents the largest CS gene pool ever found in eukaryotes so far. As comparison, most metazoans have one or two CSs. Amphioxus is the only chordate that has both the very ancient type-I CS family and the more broadly distributed type-II CS family. Specifically, amphioxus has only one type-II CS but 10–11 type-I CSs, which means that amphioxus is the only metazoan with a greatly expanded type-I CS family. Further analysis suggests that the chordate ancestor have at least one type-II CS and an expanded of type-I CS family. We hypothesize that: these ancient CSs are mostly retained in amphioxus; but the whole type-I CS family was lost in urochordates and vertebrates; the type-II CS was later duplicated into two lineages in vertebrates and followed by stochastic losses, till all type-II CSs were eventually lost in birds and mammals. Finally, our expression profiling and preliminary gene knockout analysis suggest that amphioxus CSs could have highly diverse but mildly overlapping functions in various tissues and organs.Taken together, these findings not only provide insights into the evolution of chordate CSs, lay a foundation for further functional study of the chordate CSs. After all, it is mysterious that our chordate ancestor needed so many isoenzymes for chitin formation.