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

A conserved RWP-RK transcription factor VSR1 controls gametic differentiation in volvocine algae.
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DOI:
10.1073/pnas.2305099120
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发表时间:
2023-07-18
影响因子:
11.1
通讯作者:
Umen, James
Umen, James
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Geng, Sa;Hamaji, Takashi;Ferris, Patrick J.;Gao, Minglu;Nishimura, Yoshiki;Umen, James

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性别和重组是真核生物生活史的保守特征,但性别决定机制是多样的,在大多数主要类群中知之甚少。我们的研究确定了一个长期寻求的调节性分化volvocine绿色藻类的RWP-RK家族转录因子(TF)Volvocine性别调节器1(VSR 1),导致第一个完整的范例交配型或性别决定在这个谱系。我们的研究结果支持一个模型,其中配子表达的VSR 1同源二聚化和激活加/女性特异性基因。当显性性连锁负/雄性RWP-RK家族TF MID存在时,MID-VSR 1异二聚体优先形成并激活负/雄性基因。RWP-RK TF在绿色谱系中与配子分化的广泛关联表明类似的范例可能在整个植物界中起作用。团藻绿色藻类是了解交配类型和性别进化的模型。它们是兼性的,配子分化发生在响应氮饥饿(-N)在大多数属和性诱导激素团藻。保守的RWP-RK家族转录因子(TF)MID由异宗配合的volvocine物种的负交配型位点或雄性性别决定区编码,并且主导决定负或雄性配子分化。然而,负责建立默认加或女性分化计划的因素仍然难以捉摸。我们对单细胞同花受精的莱茵衣藻(Chlamydia reinhardtii)和多细胞卵受精的团藻(Volvox carteri)在配子发生过程中诱导的常染色体RWP-RK TF进行了转录组学筛选,并确定了一个保守的邻位组,我们将其命名为Volvocine Sex Regulator 1(VSR 1)。两种交配型的衣藻vsr 1突变体都无法交配,也无法诱导关键交配型特异性基因的表达。同样,团藻vsr 1突变体在任何性别都可以启动性胚胎发生,但假定的卵子或雄配子体(精子包前体)是不育的,不能表达关键的性别特异性基因。酵母双杂交试验鉴定了VSR 1中的一个保守结构域,该结构域能够自我相互作用或与MID的保守N末端结构域相互作用。体内免疫共沉淀实验表明,在衣原体和团藻VSR 1和MID协会。这些数据支持volvocine性分化的新模型,其中VSR 1同源二聚体激活正/雌性配子特异性基因的表达,但当MID存在时,MID-VSR 1异源二聚体优先形成并激活负/雄性配子特异性基因。
Sex and recombination are conserved features of eukaryotic life cycles, but sex determination mechanisms are diverse and are poorly understood in most major taxa. Our study identified a long-sought regulator of sexual differentiation in volvocine green algae—the RWP-RK family transcription factor (TF) Volvocine Sex Regulator 1 (VSR1)—leading to the first complete paradigm for mating type or sex determination in this lineage. Our results support a model where gametically expressed VSR1 homodimerizes and activates plus/female-specific genes. When the dominant sex-linked minus/male RWP-RK family TF MID is present, MID-VSR1 heterodimers are preferentially formed and activate minus/male genes. The widespread association of RWP-RK TFs with gamete differentiation in the green lineage suggests that a similar paradigm may operate throughout the plant kingdom. Volvocine green algae are a model for understanding the evolution of mating types and sexes. They are facultatively sexual, with gametic differentiation occurring in response to nitrogen starvation (-N) in most genera and to sex inducer hormone in Volvox. The conserved RWP-RK family transcription factor (TF) MID is encoded by the minus mating-type locus or male sex-determining region of heterothallic volvocine species and dominantly determines minus or male gametic differentiation. However, the factor(s) responsible for establishing the default plus or female differentiation programs have remained elusive. We performed a phylo-transcriptomic screen for autosomal RWP-RK TFs induced during gametogenesis in unicellular isogamous Chlamydomonas reinhardtii (Chlamydomonas) and in multicellular oogamous Volvox carteri (Volvox) and identified a single conserved ortho-group we named Volvocine Sex Regulator 1 (VSR1). Chlamydomonas vsr1 mutants of either mating type failed to mate and could not induce expression of key mating-type-specific genes. Similarly, Volvox vsr1 mutants in either sex could initiate sexual embryogenesis, but the presumptive eggs or androgonidia (sperm packet precursors) were infertile and unable to express key sex-specific genes. Yeast two-hybrid assays identified a conserved domain in VSR1 capable of self-interaction or interaction with the conserved N terminal domain of MID. In vivo coimmunoprecipitation experiments demonstrated association of VSR1 and MID in both Chlamydomonas and Volvox. These data support a new model for volvocine sexual differentiation where VSR1 homodimers activate expression of plus/female gamete-specific-genes, but when MID is present, MID-VSR1 heterodimers are preferentially formed and activate minus/male gamete-specific-genes.
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