Mechanisms and evolutionary origins of germ-soma specification in a multicellular green alga, Volvox carteri

多细胞绿藻Volvox carteri生殖细胞规范的机制和进化起源

• 批准号: 1755430
• 负责人: James Umen
• 金额: $ 84.04万
• 依托单位: Donald Danforth Plant Science Center
• 依托单位国家: 美国
• 项目类别: Standard Grant
• 财政年份: 2018
• 资助国家: 美国
• 起止时间: 2018-08-01 至 2023-07-31
• 项目状态: 已结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1755430&HistoricalAwards=false
• 关键词: Mechanisms; evolutionary; origins; germ; soma

The majority of the biosphere is populated by microscopic, single-celled bacteria and protists. Yet, in a few rare instances single-celled organisms acquired the ability to aggregate or to remain associated after cell division and form collectives, thus setting the stage for the remarkable evolution of large complex multicellular life including animals, plants and a few other multicellular groups like fungi and macroalgae. This project aims to understand an important but largely mysterious step that has repeatedly occurred in conjunction with the transition to complex multicellularity: the evolution of distinct reproductive and non-reproductive cell types. In most cases this key transition is so ancient that its origins are difficult or impossible to reconstruct. By investigating cell-type specialization in a much more recently evolved multicellular species, the green alga Volvox, and comparing it to a closely-related single-celled relative, Chlamydomonas, the research team aims to understand in unprecedented genetic and genomic detail the evolutionary pathway and genetic mechanisms that enabled separate reproductive and non-reproductive cell types to arise. This project will not only address fundamental questions underlying one of evolution's most enigmatic transitions, but also has practical implications for understanding how coordinated metabolic reprogramming and specialization might be engineered into economically valuable green algae in order to tune the balance between resources allocated to cell growth versus allocation towards increased production of biofuels or high-value products that are enhanced when cell growth is minimized. The project includes graduate student and postdoctoral associate training in interdisciplinary scientific research. Outreach to local middle school students will enable students to participate in scientific discovery.The long-term goal of this research is to understand the origins and genetic mechanisms associated with multicellular organization and germ-soma division of labor. Volvox carteri 'Volvox' exhibits a streamlined and experimentally tractable form of germ-soma differentiation. Each spheroidal individual contains just two cell types: ~2000 sterile somatic cells that furnish motility and produce extracellular matrix, but which are destined to senesce and die; and ~16 large reproductive cells called gonidia, each of which undergoes a stereotyped pattern of cell divisions and morphogenesis to produce a new spheroid. It has been hypothesized that the germ-soma dichotomy in Volvox evolved by cooption of temporally-regulated and transiently-expressed differential gene expression programs from a unicellular ancestor; but this idea has not been tested on a genome-wide scale. Under this project new molecular-genetic and genomics resources will be leveraged to elucidate gene expression networks that control cell Volvox differentiation and to decipher their origins. The approaches involve: 1) Comparative analyses of cell-type transcriptomes obtained from synchronized wild-type Volvox and from cell differentiation mutants regA- and lagA- to elucidate cell-type specification networks with high spatio-temporal resolution; 2) Identification of direct targets of RegA, a nuclear-localized transcription factor and master regulator of somatic differentiation, using chromatin immunoprecipitation and deep sequencing or similar approaches; 3) Characterization and cloning of lag- mutants whose gene products suppress somatic differentiation of germ cells. Together these approaches will define the regulatory networks and control mechanisms involved in Volvox cell-type specification and critically test their origins by comparison with temporal expression programs in close relatives such as Chlamydomonas.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

生物圈的大部分由微小的单细胞细菌和原生生物组成。然而，在少数罕见的情况下，单细胞生物在细胞分裂后获得了聚集或保持联系并形成集体的能力，从而为大型复杂多细胞生命的显著进化奠定了基础，这些多细胞生命包括动物、植物和其他一些多细胞群体，如真菌和大型藻类。该项目旨在了解一个重要但很大程度上神秘的步骤，这个步骤与向复杂多细胞的过渡相结合，反复发生：不同的生殖和非生殖细胞类型的进化。在大多数情况下，这个关键的转变是如此古老，以至于很难或不可能重建它的起源。通过研究最近进化的多细胞物种绿藻的细胞类型特化，并将其与密切相关的单细胞近亲衣藻进行比较，研究小组旨在以前所未有的遗传和基因组细节了解进化途径和遗传机制，这些途径和遗传机制使不同的生殖和非生殖细胞类型出现。这个项目不仅将解决进化中最神秘的转变背后的基本问题，而且对于理解如何协调代谢重编程和专业化可能被设计成具有经济价值的绿藻，以调整分配给细胞生长的资源与分配给增加生物燃料或高价值产品的资源之间的平衡，这些资源在细胞生长最小化时得到增强，具有实际意义。本项目包括研究生和博士后跨学科科研人才培养。向当地中学生推广将使学生参与科学发现。本研究的长期目标是了解与多细胞组织和胚体分工有关的起源和遗传机制。Volvox carteri ‘Volvox’展示了一种流线型和实验上易于处理的胚体分化形式。每个球状个体只包含两种细胞类型：约2000个不育体细胞，提供运动能力并产生细胞外基质，但它们注定会衰老和死亡；还有大约16个被称为性腺的大生殖细胞，它们中的每一个都经历了一个固定的细胞分裂和形态发生模式，以产生一个新的球体。据推测，涡旋虫的胚-体细胞二分法是由单细胞祖先的暂时调节和瞬时表达的差异基因表达程序的选择而进化而来的；但是这个想法还没有在全基因组范围内进行测试。在这个项目下，新的分子遗传学和基因组学资源将被用来阐明控制细胞团藻分化的基因表达网络，并破译它们的起源。方法包括：1)对同步野生型Volvox和细胞分化突变体regA-和lagA-获得的细胞型转录组进行比较分析，以阐明高时空分辨率的细胞型规范网络；2)利用染色质免疫沉淀和深度测序或类似方法，鉴定核定位转录因子RegA的直接靶点，RegA是体细胞分化的主要调控因子；3)基因产物抑制生殖细胞体细胞分化的滞后突变体的鉴定和克隆。这些方法将共同定义与团藻细胞类型规范相关的调控网络和控制机制，并通过与近亲衣藻（Chlamydomonas）的时间表达程序进行比较，严格测试其起源。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

项目成果

A conserved RWP-RK transcription factor VSR1 controls gametic differentiation in volvocine algae.

• DOI: 10.1073/pnas.2305099120
• 发表时间: 2023-07-18
• 期刊: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• 影响因子: 11.1
• 作者: Geng, Sa;Hamaji, Takashi;Ferris, Patrick J.;Gao, Minglu;Nishimura, Yoshiki;Umen, James
• 通讯作者: Umen, James

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

• DOI: 10.1534/g3.117.300253
• 发表时间: 2018-02-02
• 期刊: G3 (Bethesda, Md.)
• 作者: Matt GY;Umen JG
• 通讯作者: Umen JG