Evolution and Mechanism of a Conserved Regulatory Switch for Mating-Types and Sexes in Volvocine Green Algae

在包括动物、植物、真菌、海藻和许多单细胞藻类和其他原生生物在内的真核生物王国中，有性繁殖和重组是生命周期和繁殖不可或缺的部分。真核生物性行为的一个标志涉及性染色体或交配型基因等遗传系统，以确保交配涉及具有两种不同交配类型或性别的个体。然而，除了动物、真菌和其他一些分类群外，关于性别和交配类型是如何确定的，或者多细胞物种中的男性和女性是如何从具有交配类型的单细胞祖先进化而来的，我们知之甚少。伏尔沃辛绿藻是一类独特的近亲，包括具有交配型的单细胞和小群体物种，以及具有性别和性染色体的较大、更复杂的物种；但它们都共享一个共同的基因系统来控制配子分化。根据这项提议，将对Volvocine藻类进行调查，以了解在进化到性别的转变中，支配交配类型的遗传系统是如何被修改的。重要的是，控制绿藻性别和交配类型的遗传机制至少部分与其他绿藻群体及其陆地植物近亲共享。因此，从这项建议中获得的知识可以影响对植物界广泛物种性别决定的理解，并可能进一步被用于培育和改良用于制造高价值生物产品或生物燃料的新兴藻类作物物种。原始真核生物是单细胞，具有等配子生殖。然而，在几乎每一个复杂的多细胞进化的谱系中，二相性也是如此--这种转变的起源和机制仍然鲜为人知。Volvocine绿藻(Chlamydomonas rehardtii、Volvox carteri及其近亲)是研究控制性别分化和两性进化的遗传网络的唯一易处理的模型。在团藻中，保守的转录因子(Tf)MID是负配子或雄配子分化的显性说明者，但导致基本性别分化的因子(S)尚不清楚。根据这一建议，将研究一种新发现的Tf，VSR1，它对于草碱藻的配子类型和性别的分化都是必不可少的。将测试和改进一个新的模型，其中VSR1同源二聚体和MID-VSR1异源二聚体之间的竞争相互作用形成性别或交配类型决定的二元开关，并将探索MID/VSR1基因调控网络(GRN)在向卵配的转变过程中扩张和分化的机制。设计的具体目标是：1)阐明和比较关键的同配子和卵配性交配代表中MID和VSR1控制配子发生的基因表达计划；2)确定VSR1中期物理相互作用的基础，以及这两个TF如何在交配基因谱系多样化期间共同进化；3)确定VSR1和MID在关键交配代表中的DNA结合特异性和直接靶标，以便能够建模与性别相关的GRN进化，并测试关于GRN在Volvox中扩展的假设。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的审查标准进行评估，被认为值得支持。

Sex and recombination are integral to life cycles and reproduction across the kingdom of eukaryotes that includes animals, plants, fungi, seaweeds and many single-celled algae and other protists. A hallmark of eukaryotic sex involves genetic systems such as sex chromosomes or mating type genes to ensure that matings involve individuals with two distinct mating types or sexes. However, outside of animals, fungi, and a few other taxa, little is known about how sexes and mating types are determined or how male and female sexes evolved in multicellular species from single-celled ancestors with mating types. Volvocine green algae are a unique group of relatives that include single celled and small colonial species with mating types, and larger more complex species with sexes and sex chromosomes; but they all share a common genetic system for controlling gamete differentiation. Under this proposal volvocine algae will be investigated to understand how the genetic systems governing mating types were modified in the evolutionary transition to sexes. Importantly, the genetic machinery that controls sexes and mating types in volvocine algae is at least partly shared with other groups of green algae and their land plant cousins. Thus, the knowledge obtained from this proposal can impact the understanding of sex determination in a wide range of species in the plant kingdom and may be further leveraged for breeding and strain improvement in emerging algal crop species that are used to make high value bioproducts or biofuels.Ancestral eukaryotes were single cells with isogamous sexual reproduction. However, in nearly every lineage where complex multicellularity evolved, so did dimorphic sexes—a transition whose origins and mechanisms remain poorly understood. Volvocine green algae (Chlamydomonas reinhardtii, Volvox carteri, and relatives) are a uniquely tractable model for investigating the genetic networks governing sexual differentiation and the evolution of dimorphic sexes. The conserved transcription factor (TF) MID is a dominant specifier of minus or male gamete differentiation in volvocine algae; but the factor(s) responsible for basal sexual differentiation as plus or female have remained unknown. Under this proposal a newly discovered TF, VSR1, that is essential for differentiation of both gamete types and sexes in volvocine algae will be investigated. A new model where competing interactions between VSR1 homodimers and MID-VSR1 heterodimers form a binary switch for sex or mating type determination will be tested and refined, and the mechanisms underlying expansion and divergence of the MID/VSR1 gene regulatory networks (GRNs) during the transition to oogamy will be explored. Specific Aims are designed to 1) Elucidate and compare the gene expression programs for gametogenesis that are governed by MID and VSR1 in key isogamous and oogamous volvocine representatives; 2) Determine the bases for MID-VSR1 physical interactions and how the two TFs co-evolved during diversification of the volvocine lineage; 3) Identify the DNA binding specificity and direct targets of VSR1 and MID in key volvocine representatives to enable modeling of sex-related GRN evolution and testing of hypotheses about GRN expansion in Volvox.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.