Cell-Type Transcriptomes of the Multicellular Green Alga Volvox carteri Yield Insights into the Evolutionary Origins of Germ and Somatic Differentiation Programs.

Cell-Type Transcriptomes of the Multicellular Green Alga Volvox carteri Yield Insights into the Evolutionary Origins of Germ and Somatic Differentiation Programs.
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DOI:
10.1534/g3.117.300253
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发表时间:
2018-02-02
期刊:
G3 (Bethesda, Md.)
影响因子:
--
通讯作者:
Umen JG
Umen JG
中科院分区:
其他
文献类型:
--
作者:
Matt GY;Umen JG

文献摘要

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生殖体分化是复杂多细胞生物的一个标志,但其起源还不清楚。团藻是一种简单的多细胞绿色藻类,最近进化出一种简单的生殖体二分法,只有两种细胞类型:大的生殖细胞称为分生孢子和小的终末分化的体细胞。在这里,我们提供了一个全面的特性的生殖器和体细胞转录组的V.卡特揭示这些细胞类型的分子和代谢编程之间的根本差异。我们发现了细胞类型之间广泛的转录组分化,体细胞表达更专业的程序在年轻的谱系特异性基因中占主导地位,而生殖腺细胞表达更通用的程序在更古老的基因中占主导地位,这些基因与动物和陆地植物的干细胞特异性基因有惊人的重叠。不同途径的定向分析揭示了细胞类型与表达生长相关基因的生殖细胞和表达面向鞭毛组装的利他代谢程序的体细胞之间的强烈二分法,鞭毛组装支持生物体运动,并将储存碳转化为糖,糖作为生产细胞外基质(ECM)糖蛋白的供体,ECM糖蛋白的分泌使生物体大规模扩张。卡氏弧菌的昼夜控制基因的直系同源物来自C. reinhardtii,一个单细胞的亲戚,进行了细胞类型分布的分析,并发现强烈的分区,与表达的暗相基因在体细胞和光相基因在分生孢子细胞中的过度代表-一个结果是一致的细胞类型程序在V. carteri产生的时间调节子的cooption在一个单细胞祖先。总之,我们的研究结果揭示了基本的分子,代谢和进化机制,这些机制是卡特氏弧菌生殖体分化起源的基础,并为理解其他多细胞谱系中生殖体分化的获得提供了模板。
Germ–soma differentiation is a hallmark of complex multicellular organisms, yet its origins are not well understood. Volvox carteri is a simple multicellular green alga that has recently evolved a simple germ–soma dichotomy with only two cell-types: large germ cells called gonidia and small terminally differentiated somatic cells. Here, we provide a comprehensive characterization of the gonidial and somatic transcriptomes of V. carteri to uncover fundamental differences between the molecular and metabolic programming of these cell-types. We found extensive transcriptome differentiation between cell-types, with somatic cells expressing a more specialized program overrepresented in younger, lineage-specific genes, and gonidial cells expressing a more generalist program overrepresented in more ancient genes that shared striking overlap with stem cell-specific genes from animals and land plants. Directed analyses of different pathways revealed a strong dichotomy between cell-types with gonidial cells expressing growth-related genes and somatic cells expressing an altruistic metabolic program geared toward the assembly of flagella, which support organismal motility, and the conversion of storage carbon to sugars, which act as donors for production of extracellular matrix (ECM) glycoproteins whose secretion enables massive organismal expansion. V. carteri orthologs of diurnally controlled genes from C. reinhardtii, a single-celled relative, were analyzed for cell-type distribution and found to be strongly partitioned, with expression of dark-phase genes overrepresented in somatic cells and light-phase genes overrepresented in gonidial cells- a result that is consistent with cell-type programs in V. carteri arising by cooption of temporal regulons in a unicellular ancestor. Together, our findings reveal fundamental molecular, metabolic, and evolutionary mechanisms that underlie the origins of germ–soma differentiation in V. carteri and provide a template for understanding the acquisition of germ–soma differentiation in other multicellular lineages.