RETINOBLASTOMA RELATED1 mediates germline entry in Arabidopsis-猫眼课题宝

DOI：

10.1126/science.aaf6532

发表时间：

2017-04

期刊：

Science

影响因子：

56.9

通讯作者：

中科院分区：

综合性期刊1区

文献类型：

作者：

Xin’Ai Zhao;Jonathan Bramsiepe;Matthias Van Durme;S. Komaki;Maria A Prusicki;Daisuke Maruyama;Joachim Forner;A. Medzihradszky;E. Wijnker;Hirofumi Harashima;You Lu;A. Schmidt;D. Guthörl;Rosa Sahún Logroño;Y. Guan;Gaëtan Pochon;U. Grossniklaus;T. Laux;T. Higashiyama;J. Lohmann;Moritz K. Nowack;A. Schnittger

与动物不同，植物不会留出生殖细胞。相反，生殖细胞是根据体细胞谱系的需要发育的。Zhao等人研究了在小型植物拟南芥中管理从体细胞到生殖细胞发育过渡的调控途径（参见Vielle-Calzada的观点）。转录因子WUSCHEL（WUS）是胚珠早期发育所必需的。不久之后，通过细胞周期蛋白依赖性激酶发挥作用的三种抑制剂允许转录阻遏物下调WUS。这打开了减数分裂的大门，同时将每粒种子的生殖单位限制在一个。《科学》，本期eaaf 6532页;另见378页细胞周期和转录因子调节将植物体细胞转化为有限数量生殖细胞的途径。开花植物的种子已经进化到通常只携带一个胚胎，旁边是一个营养组织，胚乳的功能类似于人类胎盘。这两种结构都是由一个单一的雌配子体（胚囊）形成的，在大多数有性繁殖的植物中，雌配子体是由一个减数分裂产物（功能性大孢子）发育而来的。与包括人类在内的许多其他生物一样，除了一个雌性减数分裂产物外，所有的雌性减数分裂产物都会死亡，以确保每个未来的种子只发育一个生殖单位。与人类和动物不同，植物在胚胎发生早期并没有专门的细胞谱系（生殖系）产生性母细胞。相反，植物的生殖系是从花生殖器官中的体细胞重新建立的。已经鉴定了几个控制胚珠形成的基因，胚珠是大孢子母细胞（MMCs）的港湾。这些包括同源结构域转录因子WUSCHEL（WUS），其是植物中干细胞命运的关键调节因子，对于种皮所源自的珠被的形成是必需的。此外，WUS还参与了MMC的规范制定。然而，目前尚不清楚有丝分裂的体细胞如何切换到减数分裂细胞分裂程序。结果：根据年轻胚珠原基和MMC的表达数据，我们揭示了一个控制进入减数分裂的调控级联，从一组冗余作用的细胞周期蛋白依赖性激酶（CDK）抑制剂KIP相关蛋白（KRP）类开始。KRP通过限制拟南芥视网膜母细胞瘤同源物RBR 1的CDKA;1依赖性失活发挥作用。在rbr 1和krp三突变体中，指定的性母细胞经历几次有丝分裂，导致形成额外的性母细胞，从而产生每个未来种子的多个生殖单位。现场观察表明，这些多个单位可以成功地吸引花粉管，并可以受精。然而，随后的种子发育受阻，导致突变体植物的半不育性。RBR 1的功能之一是直接抑制干细胞因子WUSCHEL（WUS），后者异位积累在三重krp和rbr 1突变体的性母细胞中。在rbr 1突变体中耗尽WUS恢复了仅单个性母细胞的形成。然而，WUS本身的异位表达不足以诱导有丝分裂而不是减数分裂，这表明RBR 1是性母细胞分化的中心枢纽。结论在WUS激活和RBR 1失活之间存在着微妙的平衡，WUS激活对胚珠原基的形成至关重要，包括珠被的发育，以及在指定MMC本身方面的作用，而RBR 1随后很快使其失活，从而进入减数分裂。Rb控制通路的不同组分与动物生殖细胞命运的起始有关;例如，果蝇中CDK抑制剂dacapo的突变体不能进入减数分裂。同样，下调Cdk 2-细胞周期蛋白E，一个众所周知的调节Rb，是很重要的秀丽隐杆线虫种系发育。这就提出了一个有趣的问题，是否Rb家族蛋白在多细胞生物的生殖细胞进入中发挥保守的作用。拟南芥中多个基质金属复合体的形成。左栏显示野生型，中栏显示krp 4、krp 6、krp 7三重突变体，右栏显示rbr 1 -2。指定的MMC经历有丝分裂而不是减数分裂，导致在三重krp和rbr 1突变体（顶行）中产生多个MMC，而不是在野生型中发现的单个MMC。MMC命运通过KNU-YFP表达突出显示（第二行）。多个MMC在胚珠中产生多个配子体（第三行，底行以不同蓝色阴影突出显示）。为了产生种子，开花植物需要指定体细胞进行减数分裂。在这里，我们揭示了一个调控级联，控制进入减数分裂开始与一组冗余的作用细胞周期蛋白依赖性激酶（CDK）抑制剂的KIP相关蛋白（KRP）类。KRP通过限制拟南芥视网膜母细胞瘤同源物RBR 1的CDKA;1依赖性失活发挥作用。在rbr 1和krp三突变体中，指定的性母细胞经历几次有丝分裂，导致形成额外的性母细胞，从而产生每个未来种子的多个生殖单位。RBR 1的一个功能是直接抑制干细胞因子WUSCHEL（WUS），后者异位积累在三重krp和rbr 1突变体的性母细胞中。在rbr 1突变体中耗尽WUS恢复了仅单个性母细胞的形成。

Germ cells on demand Unlike animals, plants do not set aside a germline. Instead, germ cells are developed on demand from somatic lineages. Zhao et al. examined the regulatory pathways that manage the transition from somatic to germ cell development in the small plant Arabidopsis (see the Perspective by Vielle-Calzada). The transcription factor WUSCHEL (WUS) was needed early on for development of ovules. Soon after, a trio of inhibitors that work through a cyclin-dependent kinase allowed a transcriptional repressor to down-regulate WUS. This opened the door to meiosis, while restricting the number of reproductive units per seed to one. Science, this issue p. eaaf6532; see also p. 378 Cell cycle and transcription factors regulate the pathway that converts plant somatic cells into a limited number of germ cells. INTRODUCTION Seeds of flowering plants have evolved to typically carry only a single embryo next to a nourishing tissue, the endosperm that functions analogously to the human placenta. Both structures are formed from a single female gametophyte (embryo sac) that develops from one meiotic product, the functional megaspore, in most sexually reproducing plants. As in many other organisms, including humans, all but one female meiotic product die to assure the development of only one reproductive unit per future seed. RATIONALE In contrast to humans and animals, plants do not set aside a specialized cell lineage (germline) that produces meiocytes in early embryogenesis. Instead, the germline of plants is established de novo from somatic cells in floral reproductive organs. Several genes have been identified that control the formation of ovules, which harbor the meiocytes [megaspore mother cells (MMCs)]. These include the homeodomain transcription factor WUSCHEL (WUS), a key regulator of stem cell fate in plants that is essential for the formation of the integuments from which the seed coat is derived. Moreover, WUS is also involved in the specification of MMCs. However, it is not clear how somatic cells that divide mitotically switch to a meiotic cell division program. RESULTS Following up expression data of young ovules primordia and MMCs, we reveal a regulatory cascade that controls the entry into meiosis, starting with a group of redundantly acting cyclin-dependent kinase (CDK) inhibitors of the KIP-RELATED PROTEIN (KRP) class. KRPs function by restricting CDKA;1–dependent inactivation of the Arabidopsis Retinoblastoma homolog RBR1. In rbr1 and krp triple mutants, designated meiocytes undergo several mitotic divisions, resulting in the formation of supernumerary meiocytes that give rise to multiple reproductive units per future seed. Live observation revealed that these multiple units can successfully attract a pollen tube and can be fertilized. However, subsequent seed development is blocked, resulting in semisterility of the mutant plants. One of the functions of RBR1 is the direct repression of the stem cell factor WUSCHEL (WUS), which ectopically accumulates in meiocytes of triple krp and rbr1 mutants. Depleting WUS in rbr1 mutants restored the formation of only a single meiocyte. However, ectopic expression of WUS by itself is not sufficient to induce mitotic divisions instead of meiosis, revealing that RBR1 is a central hub of meiocyte differentiation. CONCLUSION There is a delicate balance between WUS activation important for ovule primordia formation—including the development of the integuments, as well as a role in specifying the MMC itself—and its inactivation by RBR1 soon afterward to allow entry into meiosis. Different components of the Rb control pathway have been associated with germ cell fate initiation in animals; for example, mutants in the CDK inhibitor dacapo in Drosophila fail to enter meiosis. Similarly, down-regulation of Cdk2-cyclin E, a well-known regulator of Rb, is important for Caenorhabditis elegans germline development. This raises the intriguing question of whether Rb family proteins play a conserved role in germline entry in multicellular organisms. Formation of multiple MMCs in Arabidopsis. The left column shows the wild type, the middle column shows krp4 krp6 krp7 triple mutants, and the right column shows rbr1-2. A designated MMC undergoes a mitotic instead of a meiotic division, leading to the production of multiple MMCs in triple krp and rbr1 mutants (top row) instead of a single MMC, as found in the wild type. MMC fate is highlighted by means of KNU-YFP expression (second row). Multiple MMCs give rise to multiple gametophytes in ovules (third row and highlighted in different shades of blue in the bottom row). To produce seeds, flowering plants need to specify somatic cells to undergo meiosis. Here, we reveal a regulatory cascade that controls the entry into meiosis starting with a group of redundantly acting cyclin-dependent kinase (CDK) inhibitors of the KIP-RELATED PROTEIN (KRP) class. KRPs function by restricting CDKA;1–dependent inactivation of the Arabidopsis Retinoblastoma homolog RBR1. In rbr1 and krp triple mutants, designated meiocytes undergo several mitotic divisions, resulting in the formation of supernumerary meiocytes that give rise to multiple reproductive units per future seed. One function of RBR1 is the direct repression of the stem cell factor WUSCHEL (WUS), which ectopically accumulates in meiocytes of triple krp and rbr1 mutants. Depleting WUS in rbr1 mutants restored the formation of only a single meiocyte.

RETINOBLASTOMA RELATED1 mediates germline entry in Arabidopsis

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