Diversity of Balbiani body formation in internally and externally fertilizing representatives of Osteoglossiformes (Teleostei: Osteoglossomorpha)
体内受精和体外受精的骨舌形目（远洋鱼类：Osteoglossomorpha）代表鱼类巴尔比亚尼体形成的多样性

Department of Comparative Anatomy, Institute of Zoology and Biomedical Research, Jagiellonian University, Cracow, Poland
波兰克拉科夫雅盖隆大学动物学和生物医学研究所比较解剖学系

Rafal P. Piprek, Department of Comparative Anatomy, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Cracow, Poland. Email: rafal.piprek@uj.edu.pl
Rafal P. Piprek，波兰克拉科夫 30-387 Gronostajowa 9 号雅盖隆大学动物学和生物医学研究所比较解剖学系。电子邮件：rafal.piprek@uj.edu.pl

Ministerstwo Nauki i Szkolnictwa Wyższego, Grant/Award Number: N18/DBS/000005; PhD Students Society of Jagiellonian University; Uniwersytet Jagielloński w Krakowie, Grant/Award Number: K/ DSC/005532
Ministerstwo Nauki i Szkolnictwa Wyższego, Grant/Award Number：N18/DBS/000005; PhD Students Society of Jagiellonian University; Uniwersytet Jagielloński w Krakowie, Grant/Award Number：K/ DSC/005532

KEYWORDS 关键词

germ plasm, germline cells, mitochondria, ooplasm, previtellogenic oocytes
生殖质粒、生殖细胞、线粒体、卵原细胞、前卵母细胞

The germline is a population of cells that passes on genetic material to the progeny and thus, directly ensures the genetic continuity of a species. Germline cells proliferate and differentiate in the process of gametogenesis leading to the formation of the gametes, that is, sperm and eggs, which participate in fusion during fertilization. All germline cells originate from primordial germ cells. In some animals, these progenitor cells are specified via induction by zygotic signaling factors (induction or epigenesis), whereas in others, specification occurs by inheritance of maternally provided gene products known as the germ plasm (maternal specification or predetermination; Extavour & Akam, 2003). The germ plasm was identified in numerous model organisms including the fruit fly Drosophila melanogaster, zebrafish Danio rerio, and African clawed frog Xenopus laevis (Dosch, 2015; Illmensee & Mahowald, 1974; Tada et al., 2012). It is also known as nuage or germ granules (Gao & Arkov, 2013; Reunov, 2006), and is visible within the oocyte as irregular granules of electron-dense material typically found within mitochondria (Voronina et al., 2011). The germ plasm contains RNA and protein products of such genes as vasa, nanos, and dazl (Houston et al., 1998; Kloc et al., 2002; Knaut et al., 2000; MacArthur et al., 1999). This material is often deposited in an aggregation with organelles, forming the Balbiani body that contains mitochondria, the Golgi apparatus, endoplasmic reticulum (ER), and germ plasm (Oh & Houston, 2017). The presence of the Balbiani body was reported during the early stages of oogenesis in numerous teleosts such as Cyprinus carpio, Sciaenops ocellatus, Micropterus floridanus, Hippocampus erectus, and Millerichthys robustus (Dominguez-Castanedo & Uribe, 2019; Grier, 2012; Grier et al., 2018; Mazzoni et al., 2010; Selman & Wallace, 1989).
生殖细胞是将遗传物质传递给后代的细胞群，因此直接确保了物种遗传的连续性。生殖细胞在配子发生过程中增殖和分化，最终形成配子，即精子和卵子，并在受精过程中参与融合。所有生殖细胞都起源于原始生殖细胞。在一些动物中，这些祖细胞是通过子代信号因子的诱导（诱导或表观遗传）而形成的，而在另一些动物中，则是通过遗传母体提供的基因产物（称为生殖质）（母体规范或预定；Extavour 和 Akam，2003 年）而形成的。种质在许多模式生物中被发现，包括黑腹果蝇、斑马鱼和非洲爪蛙（Dosch，2015；Illmensee & Mahowald，1974；Tada 等人，2012）。它也被称为胚芽颗粒（nuage 或 germ granules）（Gao 和 Arkov，2013 年；Reunov，2006 年），在卵母细胞内可见不规则的电子致密物质颗粒，通常存在于线粒体内（Voronina 等人，2011 年）。胚芽质包含诸如 vasa、nanos 和 dazl 等基因的 RNA 和蛋白质产物（Houston 等人，1998 年；Kloc 等人，2002 年；Knaut 等人，2000 年；MacArthur 等人，1999 年）。这种物质通常与细胞器聚集在一起，形成包含线粒体、高尔基体、内质网（ER）和胚芽质的 Balbiani 体（Oh & Houston，2017）。据报道，在鲤鱼、Sciaenops ocellatus、Micropterus floridanus、Hippocampus erectus 和 Millerichthys robustus 等许多远洋鱼类的卵子发生早期阶段都存在 Balbiani 体（Dominguez-Castanedo & Uribe，2019；Grier，2012；Grier 等人，2018；Mazzoni 等人，2010；Selman & Wallace，1989）。

In teleosts, like in other vertebrates, the primordial germ cells migrate to the gonad anlage (genital ridges), where they terminate their migration (Piprek et al., 2016; Wootton & Smith, 2015). During sexual differentiation of the gonads, the germ cells undergo oogenesis or spermatogenesis, depending on the gonadal sex. In the ovaries during their early development, the germline cells (i.e., oogonia) enter meiosis, forming oocytes.
在长尾目动物中，与其他脊椎动物一样，原始生殖细胞迁移到性腺鞍部（生殖器脊），并在那里终止迁移（Piprek等人，2016年；Wootton和Smith，2015年）。在性腺的性分化过程中，生殖细胞会根据性腺的性别进行卵子生成或精子生成。在卵巢的早期发育过程中，生殖细胞（即卵原细胞）进入减数分裂，形成卵母细胞。

Oogonia, found in the germinal epithelium of the ovary, enter meiosis and become chromatin-nucleolus (leptotene, zygotene, pachytene, and early diplotene) oocytes. In the next stage, the primary growth (previtellogenesis) is divided into five steps (one-nucleolus, multiple-nucleoli, perinucleolar, circumnuclear oil droplets, and cortical alveolar step), which are distinguished based on the arrangement of nucleoli in the nucleus and the presence of ooplasmic inclusions, oil droplets, and cortical alveoli (Grier et al., 2009). Folliculogenesis starts when one-nucleolus oocytes relocate from the germinal epithelium to ovarian stroma. This phenomenon represents the formation of the ovarian follicle enclosed by somatic cells and the basement membrane. Subsequently, yolk accumulates in the ooplasm of the growing oocyte; this represents the next stage, namely, the secondary growth (also termed vitellogenesis). At the end of the secondary growth, the oocyte reaches its maximum diameter, matures, and becomes ready for ovulation (Juchno, Boroń, & Gołaszewski, 2007).
卵原细胞存在于卵巢的生殖上皮细胞中，进入减数分裂后，成为染色质核仁（瘦核、齐核、柏核和早期双核）卵母细胞。在下一阶段，初级生长（前卵母细胞发生）分为五个步骤（单核、多核、核周、环核油滴和皮质泡步骤），这五个步骤是根据核中核小体的排列以及卵质内含物、油滴和皮质泡的存在而区分的（Grier 等人，2009 年）。当单核卵母细胞从生殖上皮转移到卵巢基质时，卵泡生成就开始了。这一现象代表了由体细胞和基底膜包裹的卵泡的形成。随后，卵黄在不断生长的卵母细胞的卵质中积累；这代表了下一阶段，即二次生长（也称卵黄发生）。在二次发育末期，卵母细胞达到最大直径，成熟并为排卵做好准备（Juchno, Boroń, & Gołaszewski, 2007）。
The process of Balbiani body formation can be traced along the consecutive stages of fish oogenesis (Grier et al., 2009). The formation of the Balbiani body begins with its assembly around the centrosome and is noticeable as changes in the arrangement of the ooplasm (Kloc et al., 2004; Kloc et al., 2008; Kloc et al., 2014). In zebrafish D. rerio early oocytes, precursors of the Balbiani body accumulate around the centrosome. After disappearance of the centrosome, a round-shaped Balbiani body is located at the vegetal pole of the oocyte; it maintains asymmetry of the oocyte and becomes more coherent (Elkouby et al., 2016). The Balbiani body was found at the vegetal region of the germinal vesicle during early previtellogenesis also in other teleosts, such as Micropterus salmoides, M. floridanus, Syngnathus scovelli, Serrasalmus spilopleura, and antarctic fishes from the families Nototheniidae, Channichthyidae, Bathydraconidae (Begovac & Wallace, 1988; Grier et al., 2018; Guimarães & QuagioGrassiotto, 2001; Motta et al., 2005; Żelazowska & Halajian, 2019). As previtellogenesis progresses, the Balbiani body grows and eventually disperses in the ooplasm of late previtellogenic oocytes (Begovac & Wallace, 1988; Grier et al., 2018; Guimarães & QuagioGrassiotto, 2001; Motta et al., 2005; Zelazowska & Halajian, 2019).
Balbiani体的形成过程可以沿着鱼类卵子发生的连续阶段追溯（Grier等人，2009年）。Balbiani 体的形成始于其在中心体周围的组装，并明显表现为卵原细胞排列的变化（Kloc 等人，2004 年；Kloc 等人，2008 年；Kloc 等人，2014 年）。在斑马鱼 D. rerio 早期卵母细胞中，Balbiani 体的前体聚集在中心体周围。中心体消失后，圆形的 Balbiani 体位于卵母细胞的植物极；它保持了卵母细胞的不对称性，并变得更加连贯（Elkouby 等人，2016 年）。Balbiani体也出现在其他远洋鱼类的早期前细胞发生过程中的生殖泡植物区，如Micropterus salmoides、M. floridanus、Syngnathus scovelli、Serrasalmus spilopleura以及Nototheniidae、Channichthyidae、Bathydraconidae科的南极鱼类（Begovac & Wallace, 1988; Grier et al、2018；Guimarães & QuagioGrassiotto, 2001；Motta 等人，2005；Żelazowska & Halajian, 2019）。随着前细胞发生的进展，Balbiani体不断生长，并最终分散到晚期前细胞发生卵母细胞的卵质中（Begovac & Wallace, 1988; Grier等人，2018; Guimarães & QuagioGrassiotto, 2001; Motta等人，2005; Żelazowska & Halajian, 2019）。

The Balbiani body is an important structure that is supposed to optimize the oocyte condition for the future development of the embryo across a wide range of bony fishes. However, its form varies significantly, and it may present as a single round mass (e.g., in zebrafish D. rerio, Triacanthus brevirostris, Ambassis gymnocephalus, and Oncorrhynhus mykiss), as an irregular body (as in notothenioids), or as unevenly distributed irregular structures (e.g., in C. carpio; Chaudhry, 1952; Fishelson & Gon, 2009; Fusco et al., 2000; Lowry et al., 2005; Marlow & Mullins, 2008; Mazzoni et al., 2010). Moreover, in Acipenser gueldenstaedtii, components of the Balbiani body are dispersed within one zone of the ooplasm called Balbiani cytoplasm (Żelazowska et al., 2007). The diversity of the Balbiani body among species may suggest that it is a flexible oocyte structure. So far, studies on Balbiani body formation focused on species with external fertilization, which is observed in of teleost species. However, it remains to be elucidated whether Balbiani body formation differs between species with various types of fertilization belonging to the same family. We previously described the diversity in ovarian structure and ooplasm arrangement in previtellogenic oocytes of some osteoglossiform species (Dymek et al., 2021), which may suggest that also Balbiani body formation is evolutionarily malleable.
Balbiani体是一种重要的结构，其作用是优化卵母细胞的状态，以利于各种有骨鱼类胚胎的未来发育。然而，其形态差异很大，可能表现为单个圆形体块（如斑马鱼 D. rerio、Triacanthus brevirostris、Ambassis gymnocephalus 和 Oncorrhynhus mykiss），也可能表现为不规则体块（如蝾螈类），或分布不均的不规则结构（如鲤科鱼类；Chaudhry，2006 年）、Chaudhry, 1952; Fishelson & Gon, 2009; Fusco 等人, 2000; Lowry 等人, 2005; Marlow & Mullins, 2008; Mazzoni 等人, 2010）。此外，在鲟鱼（Acipenser gueldenstaedtii）中，Balbiani 体的组成部分分散在称为 Balbiani 细胞质的卵质区（Żelazowska 等人，2007 年）。Balbiani体在物种间的多样性可能表明它是一种灵活的卵母细胞结构。迄今为止，有关 Balbiani 体形成的研究主要集中在具有外部受精的物种上，这在 的远摄鱼类物种中可以观察到。然而，Balbiani体的形成在同一科具有不同受精类型的物种之间是否存在差异仍有待阐明。我们之前描述了一些骨舌鱼类物种卵巢结构和卵原细胞前质排列的多样性（Dymek等人，2021年），这可能表明Balbiani体的形成在进化过程中也是可塑的。

Osteoglossomorpha, one of the three most basal groups of Teleostei (Hilton & Lavoué, 2018), exhibits diversity in reproductive biology, practicing either internal or external fertilization, which is reflected in sperm structure. Pantodon buchholzi (Pantodontidae), the only extant osteoglossomorph with insemination, produces complex introsperm packed into naked bundles (spermatozeugmata), whereas all other species classified into this group produce sperm releasing into water, called aquasperm, which is categorized as uniflagellate, biflagellate, and aflagellate (Mattei, 1970, 1991; Mattei et al., 1967; Mattei et al., 1972; Mattei et al., 2019; van Deurs, 1973; van Deurs & Lastein, 1973). This suggests that . buchholzi may be the most basal teleost species in which insemination has evolved (Dymek &
骨龙目（Osteoglossomorpha）是长尾目（Teleostei）中最基干的三个类群之一（Hilton & Lavoué，2018年），在生殖生物学方面表现出多样性，实行体内或体外受精，这反映在精子结构上。Pantodon buchholzi（Pantodontidae）是现存唯一具有人工授精功能的骨龙目动物，其产生的内精子结构复杂，成裸束状（spermatozeugmata），而该类群的所有其他物种都产生释放到水中的精子，称为水精子，分为单鞭毛、双鞭毛和黄鞭毛（Mattei，1970，1991；Mattei et al、1967；Mattei 等人，1972；Mattei 等人，2019；van Deurs，1973；van Deurs & Lastein，1973）。这表明 . buchholzi 可能是人工授精进化的最基础的远洋鱼类物种（Dymek & Lastein, 1973）。

Pecio, 2019). The process of spermatogenesis in this species leads to the formation of one of the most complex introsperm among fish. It also reveals some unique features, such as degradation of an enormous number of Golgi complexes as spindle-shaped bodies, being the main component of residual bodies (Dymek & Pecio, 2020). Considering the great variation of the spermatozoa and their unique features in Osteoglossomorpha, the question remains whether there is comparable diversity in female gamete development.
Pecio，2019 年）。该物种的精子发生过程会形成鱼类中最复杂的精子。它还显示出一些独特的特征，如大量高尔基复合体退化为纺锤形体，成为残留体的主要组成部分（Dymek & Pecio, 2020）。考虑到大骨节虫精子的巨大差异及其独特特征，问题仍然是雌配子的发育是否存在类似的多样性。

The aim of this study was to examine the development of the Balbiani body during oogenesis in three teleost species, representatives of Osteoglossiformes: the internally fertilizing freshwater butterflyfish P. buchholzi (Pantodontidae) from West Africa and the externally fertilizing silver arowana Osteoglossum bicirrhosum and pirarucu Arapaima gigas (Osteoglossidae) from South America. The second aim was to investigate if there are any differences in the Balbiani body possibly linked with reproductive biology.
本研究的目的是研究三种远东鱼类（骨舌鱼类的代表）在卵子发生过程中巴尔比亚尼体的发育情况：西非的内部受精淡水蝶鱼（Pantodontidae）和南美洲的外部受精银箭鱼（Osteoglossum bicirrhosum）和巨嘴鸟（Osteoglossidae）。第二个目的是调查 Balbiani 的身体是否存在任何可能与生殖生物学有关的差异。

Three females of each species, Pantodon buchholzi (Peters, 1877), Osteoglossum bicirrhosum (Cuvier, 1829), and Arapaima gigas (Schinz, 1822), obtained from a local aquarium shop, were euthanized by immersion in a solution of tricaine methanesulfonate (MS-222). The females of each species were during the early phase of ovary development: P. buchholzi, mean standard length of the specimens . bicirrhosum, mean standard length of the specimens ; and . gigas, mean standard length of the specimens . This study was conducted according to the Act on the Protection of Animals Used for Scientific or Educational Purposes (Dz.U. 2015 poz. 266).
将从当地水族店获得的 Pantodon buchholzi（Peters，1877 年）、Osteoglossum bicirrhosum（Cuvier，1829 年）和 Arapaima gigas（Schinz，1822 年）各物种的三条雌鱼浸泡在 的甲磺酸三卡因溶液（MS-222）中实施安乐死。每个物种的雌鱼都处于卵巢发育的早期阶段：P. buchholzi，标本的平均标准长度 。 bicirrhosum，标本的平均标准长度 ；以及 。 gigas，标本的平均标准长度 。本研究根据《科学或教育用途动物保护法》（Dz.U. 2015 poz. 266）进行。

The ovaries were dissected, cut into pieces, and fixed for in a mixture of glutaraldehyde and paraformaldehyde in phosphate buffer ( ) and postfixed for 30 min in osmium tetroxide in phosphate buffer. Then, the samples were dehydrated in a graded alcohol series, embedded in Epon 812, and cut into semithin and ultrathin sections as previously described (Dymek & Pecio, 2020). Semithin sections stained with a mixture of azure II and methylene blue (1:1) were viewed under a light microscope and photographed using a Nikon COOLPIX P6000 camera. Ultrathin sections contrasted with uranyl acetate and lead citrate were examined using a JEM-2100HT (JEOL ) transmission electron microscope. Images were taken by software associated with the microscope.
解剖卵巢，切成小块，在 戊二醛和 多聚甲醛在磷酸盐缓冲液中的混合物中固定 ( )，然后在 四氧化锇在磷酸盐缓冲液中固定 30 分钟。然后，样本在分级酒精系列中脱水，包埋在 Epon 812 中，并按照之前的描述切成半薄和超薄切片（Dymek & Pecio，2020 年）。用天青 II 和亚甲基蓝（1:1）混合物染色的半薄切片在光学显微镜下观察，并用尼康 COOLPIX P6000 相机拍照。使用 JEM-2100HT (JEOL ) 透射电子显微镜观察醋酸铀酰和柠檬酸铅对比的超薄切片。图像由显微镜的相关软件拍摄。

In each step of oogenesis 25 cells were measured (diameter for round cells or longitudinal and lateral axis of a fitted ellipse for oval cells) using
在卵子发生的每一个阶段，都要对 25 个细胞进行测量（圆形细胞测量直径，椭圆形细胞测量拟合椭圆的纵轴和横轴）。
ImageJ V 1.8.0 (Schneider, Rasband, & Eliceiri, 2012). Then mean dimensions with SD were calculated using MS Excel (Microsoft Corporation).
ImageJ V 1.8.0（Schneider、Rasband 和 Eliceiri，2012 年）。然后使用 MS Excel（微软公司）计算平均尺寸和标度。

In the ovaries of Pantodon buchholzi, Osteoglossum bicirrhosum, and Arapaima gigas, germ cells in the following stages were observed: primary and secondary oogonia, zygotene, pachytene and diplotene oocytes, as well as previtellogenic oocytes. In our study, we focused on assessing the ultrastructure of the nucleus and ooplasm, with particular emphasis on Balbiani body components. At the consecutive stages of oogenesis, some interspecific differences in the organization of the Balbiani body were observed.
在 Pantodon buchholzi、Osteoglossum bicirrhosum 和 Arapaima gigas 的卵巢中，我们观察到处于以下阶段的生殖细胞：初级和次级卵原细胞、子代卵母细胞、柏氏卵母细胞和二分裂卵母细胞，以及前卵细胞。在研究中，我们重点评估了细胞核和卵原细胞的超微结构，尤其是巴比体成分。在卵子发生的连续阶段，我们观察到Balbiani体的组织结构存在一些种间差异。

Primary oogonia, which divide mitotically, were located within the germinal epithelium in all three studied species (Figure 1a-c). They were individual spherical cells with oval nucleus and one spherical nucleolus. Mean diameter of primary oogonia was in P. buchholzi, in 0 . bicirrhosum and in . gigas. Within the ooplasm, evenly distributed mitochondria, ER, and prominent Golgi apparatus were observed (Figure 1d). After incomplete cytokinesis following karyokinesis during mitotic divisions, secondary oogonia with oval nucleus and one or two spherical nucleoli were arranged in germ cell nests (Figure 1a-c). Their mean diameter was in P. buchholzi, in 0 . bicirrhosum and in A. gigas. In P. buchholzi and O. bicirrhosum, secondary oogonia exhibited similar ooplasmic organization to primary oogonia. However, in A. gigas, the smooth ER took different forms: karmellae (i.e., long stacks of membranes, partially enclosing the nucleus) or tightly packed whorls of lamellae (Figure 1e).
有丝分裂的初级卵原细胞位于所有三个研究物种的生殖上皮细胞内（图 1a-c）。它们是单个球形细胞，具有椭圆形细胞核和一个球形核仁。初级卵原细胞的平均直径在布氏栉水母中为 ，在 0 . bicirrhosum 中为 ，在 . gigas 中为 。在卵原细胞内，可以观察到均匀分布的线粒体、ER 和突出的高尔基体（图 1d）。在有丝分裂过程中，核分裂后细胞运动不完全，次生卵原细胞具有椭圆形核和一个或两个球形核小体，排列在生殖细胞巢中（图 1a-c）。它们的平均直径在 P. buchholzi 中为 ，在 0. bicirrhosum 中为 ，在千足虫中为 。在 P. buchholzi 和 O. bicirrhosum 中，次级原核表现出与初级原核相似的质体组织。然而，在千足虫中，光滑的ER具有不同的形式：karmellae（即长的膜堆，部分包围细胞核）或紧密排列的片层（图1e）。

Secondary oogonia entering meiosis differentiated into chromatin-nucleolus oocytes that exhibited similar diameter as in previous step. In the leptotene oocytes, the chromosome condensation began (Figure 2a). In P. buchholzi and A. gigas, the ooplasm of the leptotene oocytes organization was similar as in the previous step, but in O. bicirrhosum, it exhibited a distinguished form of the ER, seen in the ooplasm as the annulate lamellae, which are stacked parallel membranes with numerous pores and are located close to the nuclear envelope (Figure 2a).
进入减数分裂的次级卵原细胞分化成染色质核仁卵母细胞，其直径与上一步相似。在瘦核卵母细胞中，染色体开始凝结（图 2a）。在 P. buchholzi 和 A. gigas 中，单核卵母细胞的卵原组织与上一步相似，但在 O. bicirrhosum 中，卵原组织中的ER形态不同，表现为环状薄片，这些薄片是堆叠的平行膜，有许多孔，靠近核膜（图 2a）。

In the zygotene oocytes of all studied species, homologous chromosomes became visible in the nucleus (Figure 2b). In P. buchholzi and A. gigas, mitochondria, the Golgi apparatus and ER were irregularly dispersed throughout the ooplasm, around the centrally located nucleus with no signs of asymmetry (Figure 2b,c). In A. gigas, some vesicles were also present, which were irregularly distributed within the ooplasm (Figure 2b,c). In O. bicirrhosum, polarization reflected by the location of the nucleus at one pole of the cell and organelles at
在所有研究物种的合子卵母细胞中，细胞核内均可见同源染色体（图 2b）。在布氏杆菌和千足虫中，线粒体、高尔基体和ER不规则地分布在整个卵原细胞中，围绕着位于中心的细胞核，没有不对称的迹象（图 2b、c）。在千足虫中，也存在一些囊泡，它们不规则地分布在卵原细胞中（图 2b、c）。在 O. bicirrhosum 中，细胞核位于细胞的一极，细胞器位于细胞的二极，这反映了极化现象。

FIGURE 1 Germinal epithelium and ultrastructure of primary and secondary oogonia in Pantodon buchholzi (a), Osteoglossum bicirrhosum (b, d), Arapaima gigas (c, e). (a-c) Semithin sections through the ovary fragments. In the germinal epithelium, primary oogonia are visible as single cells, whereas secondary oogonia form the nests (encircled by dotted line).
图 1 Pantodon buchholzi（a）、Osteoglossum bicirrhosum（b，d）和 Arapaima gigas（c，e）的生殖上皮以及初级和次级卵原细胞的超微结构。(a-c）卵巢碎片的半切片。在生殖上皮细胞中，单细胞可见初级卵原细胞，而次级卵原细胞则形成巢（虚线环绕）。

(d) Ultrastructure of the primary oogonium. (e) Ultrastructure of the secondary oogonium. ER, endoplasmic reticulum; GA, Golgi apparatus; Kr, karmellae; , lumen; , mitochondrion; , nucleus; Nu, nucleolus; pFC, prefollicular cell; POg, primary oogonia; SOg, secondary oogonia; Wh, whorl the opposite side was observed (Figure 2d). In this species, oval accumulations of the nuclear material (precursors of the germ plasm) were seen close to the nuclear envelope, whereas germ plasm, visible as electron-dense granular structures surrounded by mitochondria (Figure 2d,e) as well as the complexes of the Golgi apparatus (Figure 2f), appeared in the ooplasm of the zygotene oocytes.
(d) 初级气孔的超微结构。(e) 次生骨膜的超微结构。ER，内质网；GA，高尔基体；Kr，核膜； ，管腔； ，线粒体； ，细胞核；Nu，核仁；pFC，前叶细胞；POg，初级卵原细胞；SOg，次级卵原细胞；Wh，轮生细胞。在该物种中，核物质（胚芽质的前体）的椭圆形堆积物靠近核膜，而胚芽质则出现在合子卵母细胞的卵质中，可见线粒体（图 2d、e）和高尔基体复合物（图 2f）包围的电子致密颗粒结构。

The pachytene was characterized by the presence of synaptonemal complexes in the nucleus (Figure ). In . buchholzi and O. bicirrhosum, cellular organization seemed to be similar as described for the previous step; however, in A. gigas, some differences were observed. Pachytene oocytes in A. gigas showed polarization with mitochondria and the ER on one side of the cell and with nucleus on the opposite side (Figure ). Electron-dense, irregularly shaped nuclear material passed through the nuclear envelope (Figure ), and then was seen in the ooplasm as more or less oval assembly of the germ plasm (Figure ). The cross sections obtained from . gigas revealed that the germ plasm is formed by highly electron-dense material located peripherally and surrounding medium electron-dense material. One, or sometimes two such assemblies of the germ plasm were located in the ooplasm near the nucleus (Figure 2h,i), and the electron-dense material was observed in close contact with mitochondria forming a cluster (Figure 2i). Mitochondria were surrounded by ER.
突变体的特征是细胞核中存在突触复合体（图 ）。在 . buchholzi 和 O. bicirrhosum 中，细胞组织似乎与前一步描述的相似；但在千足金枪鱼中，观察到了一些差异。千足虫的卵母细胞呈两极分化，线粒体和细胞内质网位于细胞的一侧，细胞核位于细胞的另一侧（图 ）。电子致密、形状不规则的核物质穿过核膜（图 ），然后在卵质中看到或多或少椭圆形的种质集合体（图 ）。从 . gigas 获得的横截面显示，种质是由位于外围的高电子密度物质和周围的中等电子密度物质形成的。在靠近细胞核的卵质中，有一个或有时有两个这样的种质集合体（图 2h、i），电子致密物质与线粒体紧密接触，形成一个线粒体簇（图 2i）。线粒体被ER包围。

During the primary growth, oocytes increased their size and their ooplasmic organization visibly changed. The components of the Balbiani body, which had a different arrangement during the early primary growth of studied species, ultimately dispersed evenly in the ooplasm at the beginning of the cortical alveolar step.
在初级生长过程中，卵母细胞的体积增大，卵质组织发生了明显变化。在所研究物种的初级生长早期，巴尔比亚尼体的各组成部分有着不同的排列方式，而在皮层肺泡阶开始时，这些组成部分最终会均匀地分散在卵质体中。

In all three studied species, PGon oocytes were still visible in the vicinity of the secondary oogonia. Their mean diameter was 10.67 in P. buchholzi, in 0 . bicirrhosum and 12.58 in A. gigas. The oocytes at this step contained oval nucleus with one round nucleolus (Figure 3). In P. buchholzi, the PGon oocyte was filled with highly electron-dense ooplasm, in which the mitochondria, ER (Figure 3a) and a number of Golgi apparatus surrounded the nucleus. In . bicirrhosum and . gigas, the ooplasm was electronlucent and contained dispersed ER (Figure 3b,c) and a number of Golgi apparatus. In O. bicirrhosum, mitochondria were dispersed (Figure 3b), whereas in A. gigas, they were still visible in the cluster (Figure 3c).
在所有研究的三个物种中，次级卵原细胞附近仍能看到 PGon 卵母细胞。它们的平均直径分别为：布霍尔子（P. buchholzi）为 10.67 ，比西弗斯（0. bicirrhosum）为 ，千足巨人（A. gigas）为 12.58 。这一步的卵母细胞含有椭圆形核和一个圆形核仁（图 3）。在 P. buchholzi 中，PGon 卵母细胞充满高度电子致密的卵质，其中线粒体、ER（图 3a）和一些高尔基体包围着细胞核。在 . bicirrhosum 和 . gigas 中，卵质呈电子透明状，包含分散的 ER（图 3b,c）和一些高尔基体。在 O. bicirrhosum 中，线粒体是分散的（图 3b），而在千足虫中，线粒体在团块中仍然可见（图 3c）。

In the PGmn oocyte, numerous nucleoli were dispersed evenly within the nucleoplasm (Figure 4a). During this step, the most distinct changes in oocyte organization were visible in . buchholzi (Figure 4). In this species, early PGmn oocytes ) were filled with two types of ooplasm: highly electrondense ooplasm dominating in the whole oocyte, and medium electron-dense ooplasm located at one pole of the nucleus (Figure 4a-c). Besides highly and medium electron-dense ooplasm, the third type of ooplasm, electron translucent, began to appear
在 PGmn 卵母细胞中，大量核小体均匀分布在核质中（图 4a）。在这一过程中， . buchholzi 的卵母细胞组织发生了最明显的变化（图 4）。在该物种中，早期 PGmn 卵母细胞 )充满了两种类型的卵原质：在整个卵母细胞中占主导地位的高电子致密卵原质和位于细胞核一极的中等电子致密卵原质（图 4a-c）。除了高电子密度和中等电子密度的卵原细胞外，还开始出现第三种类型的卵原细胞，即电子半透明卵原细胞

FIGURE 2 Ultrastructure of chromatin-nucleolus oocytes of Osteoglossum bicirrhosum (a, d-f) and Arapaima gigas (b, c, g-i). (a) Fragment of leptotene oocyte. (b) Ultrastructure of zygotene oocyte. (c) Details from (b). (d) Zygotene oocyte with the nucleus located at one pole of the cell and accumulation of the germ plasm surrounded by mitochondria at the opposite side of the cell. (e) Fragment of zygotene oocyte with granular germ plasm surrounded by mitochondria within the ooplasm. (f) Fragment of zygotene oocyte with the complex of the Golgi apparatus present in the ooplasm. (g-i) Pachytene oocytes with the nucleus located at one pole of the cell and the cluster of mitochondria at the opposite side. (g) Irregularly shaped nuclear material passes through the nuclear envelope. (inset) Details of the nuclear material, which is present on both sides of the nuclear envelope. (h) Oval accumulation of the germ plasm is seen near the nucleus. (inset) Details of the germ plasm. (i) The germ plasm is located close to the mitochondria. A section through this structure reveals that it consists of peripherally located, highly electron-dense material, which surrounds medium electron-dense material. (inset) Close contact of the germ plasm and mitochondrion. AL, annulate lamellae; Ch, chromosomes; ER, endoplasmic reticulum; GA, Golgi apparatus; GP, germ plasm; HC, homologous chromosomes; M, mitochondrion; N, nucleus; NM, nuclear material; SC, synaptonemal complexes; , vesicles
图 2 双棘鲷(a, d-f) 和千岛鲷(b, c, g-i) 染色质-核仁卵母细胞的超微结构。(a）瘦卵母细胞片段。(b) 子代卵母细胞的超微结构。(c) (b)中的细节。(d) 长子卵母细胞，细胞核位于细胞的一极，生殖质堆积在细胞的另一侧，由线粒体包围。(e) 子代卵母细胞片段，卵质内有颗粒状胚芽质，周围有线粒体。(f) 子代卵母细胞片段，卵质内有高尔基体复合体。(g-i）长卵母细胞，细胞核位于细胞的一极，线粒体群位于细胞的另一侧。(g）形状不规则的核物质穿过核膜。(插图）核物质的细节，存在于核膜两侧。(h) 核附近可见椭圆形的生殖质堆积。(插图）胚芽质的细节。(i) 胚芽质靠近线粒体。该结构的切面显示，它由位于外围的高电子密度物质组成，周围是中等电子密度物质。(插图）胚芽质与线粒体紧密接触。AL，环状薄片；Ch，染色体；ER，内质网；GA，高尔基体；GP，种质；HC，同源染色体；M，线粒体；N，细胞核；NM，核物质；SC，突触复合体； ，囊泡

FIGURE 3 Ultrastructure of one-nucleolus oocytes in Pantodon buchholzi (a), Osteoglossum bicirrhosum (b), and Arapaima gigas (c). (a) Onenucleolus oocyte filled with highly electron-dense ooplasm (I). (inset) Fragment of one-nucleolus oocyte with mitochondria and endoplasmic reticulum seen in highly electron-dense ooplasm (I). (b) One-nucleolus oocyte filled with electron translucent ooplasm, in which elongated mitochondria and the endoplasmic reticulum are dispersed. (c) One-nucleolus oocyte filled with electron translucent ooplasm, in which the nucleus is located at one pole of the cell and cluster of mitochondria at the opposite side. ER, endoplasmic reticulum; FC, follicular cells; M, mitochondrion; N, nucleus; Nu, nucleolus; I, highly electron-dense ooplasm
图 3 Pantodon buchholzi（a）、Osteoglossum bicirrhosum（b）和 Arapaima gigas（c）单核卵母细胞的超微结构。(a）充满高电子密度卵原质的单核卵母细胞（I）。(插图）单核卵母细胞片段，高电子密度卵原质中可见线粒体和内质网（I）。(b) 单核卵母细胞充满电子半透明卵质，其中线粒体和内质网分散。(c) 充满电子半透明卵质的单核卵母细胞，细胞核位于细胞的一极，线粒体群位于细胞的另一侧。ER，内质网；FC，卵泡细胞；M，线粒体；N，细胞核；Nu，核仁；I，高度电子致密的卵质

FIGURE 4 Structure and ultrastructure of early and late multiple-nucleoli oocytes in Pantodon buchholzi. (a) Semithin section of the early multiple-nucleoli oocyte filled with three types of ooplasm. (b) Fragment of the early multiple-nucleoli oocyte, in which mitochondria and accumulation of the endoplasmic reticulum are found in highly-electron dense ooplasm (I). (c) Fragment of the early multiple-nucleoli oocyte with two types of ooplasm visible (d). Fragment of the early multiple-nucleoli oocyte, in which the accumulation of nuclear material is found peripherally in the nucleus and numerous accumulations of the germ plasm are found in the ooplasm, close to the nuclear envelope, as well as surrounded by mitochondria. (e) Semithin section of the late multiple nucleoli oocyte filled with three types of ooplasm. Volume of electron translucent ooplasm (III) increases in the oocyte. (f) Fragment of the oocyte in which numerous accumulations of the germ plasm are surrounded by mitochondria and the endoplasmic reticulum is scattered among them. (g) Fragment of the oocyte in which numerous round accumulations of the germ plasm are located in medium electron-dense ooplasm. ER, endoplasmic reticulum; GP, germ plasm; M, mitochondrion; N, nucleus; NM, nuclear material; , nucleolus; I, highly-electron dense ooplasm; II, medium electron-dense ooplasm; III, electron translucent ooplasm
图 4 Pantodon buchholzi 早期和晚期多核卵母细胞的结构和超微结构。(a) 早期多核卵母细胞的半薄切片，其中充满了三种类型的卵原细胞。(b）早期多核卵母细胞片段，其中线粒体和内质网堆积在高电子密度的卵原细胞中（I）。(c）早期多核卵母细胞片段，可见两种类型的卵原质（d）。早期多核卵母细胞片段，其中核物质堆积在细胞核外围，大量胚质堆积在靠近核膜的卵原质中，并被线粒体包围。(e) 充满三种卵质的晚期多核卵母细胞半切片。电子半透明卵原细胞（III）的体积随着卵母细胞的增大而增大。(f) 卵母细胞片段，其中大量胚芽质堆积被线粒体包围，内质网散布其中。(g) 卵母细胞片段，其中大量圆形胚芽质堆积位于中等电子密度的卵原质中。ER，内质网；GP，胚质；M，线粒体；N，细胞核；NM，核物质； ，核仁；I，高电子密度卵质；II，中等电子密度卵质；III，电子半透明卵质。
peripherally (Figure 4a). The nucleus and medium electron-dense ooplasm were surrounded by mitochondria scattered across the accumulation of the ER (Figure 4a,b). The lamellae of the ER were observed in close contact with mitochondria (Figure 4B) forming mitochondria-associated membranes. In the nucleus, irregularly shaped electron-dense nuclear material was visible near the nuclear envelope, whereas in the ooplasm, numerous round accumulations of the germ plasm were seen close to the nucleus as well as associated with mitochondria (Figure 4d). In late PGmn oocytes (39.89 ) of . buchholzi, the volume of electron translucent ooplasm increased and was visible in different areas of the cell (Figure 4e), whereas the germ plasm was observed in close contact with mitochondria forming a cluster in highly electron-dense ooplasm (Figure 4f) and was seen as round structures in medium electrondense ooplasm (Figure 4g).
外围（图 4a）。细胞核和中等电子密度的细胞质被线粒体包围，线粒体散布在ER的积聚处（图4a,b）。观察到ER的片层与线粒体紧密接触（图4b），形成线粒体相关膜。在细胞核中，核膜附近可见形状不规则的电子致密核物质，而在卵质中，细胞核附近可见许多圆形的生殖质堆积，并与线粒体相关（图 4d）。在 . buchholzi 的晚期 PGmn 卵母细胞（39.89 ）中，电子半透明卵原质的体积增大，在细胞的不同区域均可见（图 4e），而在高电子密度卵原质中可观察到胚芽质与线粒体密切接触，形成一簇（图 4f），在中等电子密度卵原质中则可见圆形结构（图 4g）。

In O. bicirrhosum and . gigas, the PGmn oocytes (29.73 in O bicirrhosum; in . gigas) were filled with electron translucent ooplasm only, in which mitochondria formed clusters visible in the cross section of the oocyte as usually two clusters in O. bicirrhosum or one cluster in A. gigas (Figure 5a,b). Within a cluster, numerous mitochondria interconnected into the mitochondrial network were joined with the germ plasm that formed strings in O. bicirrhosum (Figure 5c) or aggregations in A. gigas (Figure 5d).
在 O. bicirrhosum 和 . gigas 中，PGmn 卵母细胞（在 O. bicirrhosum 中为 29.73 ；在 . gigas 中为 ）只充满了电子半透明卵质，其中线粒体形成的线粒体团在卵母细胞横截面上可见，在 O. bicirrhosum 中通常为两个线粒体团，在 A. gigas 中通常为一个线粒体团（图 5a,b）。在一个线粒体簇内，许多线粒体相互连接成线粒体网络，并与种质相连接，在双壳卵母细胞中形成串状（图 5c），在千足虫中形成聚合体（图 5d）。

During the PGpn, spherical nucleoli were located peripherally in the nucleus. At this step, in oocytes of . buchholzi ), the ER dispersed, whereas mitochondria formed numerous independent clusters cemented by germ plasm, located in electron-dense ooplasm (Figure 6a). Previously described round aggregations of the germ plasm present in medium electron-dense ooplasm were now seen as numerous "net-like" structures (Figure 6b). A volume of electron translucent ooplasm increased during this step (not shown).
在 PGpn 期间，球形核小体位于细胞核外围。在这一步，在 . buchholzi ）的卵母细胞中，内质网分散，而线粒体则形成了许多由胚芽质粘合的独立簇，位于电子致密的卵质中（图 6a）。以前描述的中电子密度卵质中的胚芽质圆形聚集体现在被看作是许多 "网状 "结构（图 6b）。在这一步骤中，电子半透明卵质的体积有所增加（图中未显示）。
FIGURE 5 Structure of multiple-nucleoli oocyte and ultrastructure of the mitochondrial nets in Osteoglossum bicirrhosum ( ) and Arapaima gigas (b, d). (a) Semithin section of multiple-nucleoli oocyte in which two mitochondrial nets are present in the ooplasm. (b) Semithin section of multiple-nucleoli oocyte with one mitochondrial net located in the ooplasm. (c) Ultrastructure of the mitochondrial net with accumulations of the germ plasm that form strings between fused mitochondria.
图 5 Osteoglossum bicirrhosum ( ) 和 Arapaima gigas (b, d) 的多核卵母细胞结构和线粒体网的超微结构。(a）多核卵母细胞半薄切片，其中卵质中有两个线粒体网。(b）多核卵母细胞半薄切片，卵质中有一个线粒体网。(c）线粒体网的超微结构，在融合的线粒体之间有胚芽质积聚成串。

(d) Ultrastructure of the mitochondrial net with accumulations of the germ plasm present between fused mitochondria. GP, germ plasm; M, mitochondrion; star, mitochondrial nets
(d) 线粒体网的超微结构，融合的线粒体之间存在种质堆积。GP，胚芽质；M，线粒体；星形，线粒体网

FIGURE 6 Ultrastructure of parts of the perinucleolar oocytes of Pantodon buchholzi (a, d), Osteoglossum bicirrhosum (b, e), and Arapaima gigas (c, f). (a) Fragment of the oocyte in which accumulations of the germ plasm are surrounded by mitochondria forming a cluster. (b) Fragment of the oocyte in which accumulations of the germ plasm located in medium electron-dense ooplasm (II) form "net-like" structures. (c) Fragment of the oocyte with dispersed mitochondria and Golgi apparatus in electron translucent ooplasm. A small part of a network formed by the endoplasmic reticulum is visible. (d) Part of the ooplasm of the oocyte with a network formed by the endoplasmic reticulum. (e) Fragment of the oocyte with numerous lysosome-like bodies visible in the ooplasm. (f) Fragment of the oocyte in which accumulations of the germ plasm are visible close to the mitochondria. CA, cortical alveolus; ER, endoplasmic reticulum; FC, follicular cell; GA, Golgi apparatus; GP, germ plasm; LB, lysosome-like body; M, mitochondrion; N, nucleus; Nu, nucleolus; I, highly-electron dense ooplasm; II, medium electron-dense ooplasm
图 6 Pantodon buchholzi（a，d）、Osteoglossum bicirrhosum（b，e）和 Arapaima gigas（c，f）核周卵母细胞的部分超微结构。(a）卵母细胞片段，其中胚芽质堆积被线粒体包围，形成一个线粒体团。(b) 卵母细胞片段，其中位于中等电子密度卵原质（II）中的种质堆积形成 "网状 "结构。(c) 线粒体和高尔基体分散在电子半透明卵质中的卵母细胞片段。可见内质网形成的网状结构的一小部分。(d) 卵母细胞的部分卵原质与内质网形成的网络。(e) 卵质中可见大量溶酶体样体的卵母细胞片段。(f）卵母细胞片段，其中可见靠近线粒体的生殖质堆积。CA，皮质泡；ER，内质网；FC，卵泡细胞；GA，高尔基体；GP，种质；LB，溶酶体样体；M，线粒体；N，细胞核；Nu，核仁；I，高电子密度卵质；II，中等电子密度卵质。

Within the PGpn oocytes of . bicirrhosum , mitochondria began to disperse within the entire volume of the electron translucent ooplasm, but the ER formed a network that was located near the nucleus (Figure 6c,d). In the ooplasm, numerous lysosome-like bodies were also present, visible as round lamellar structures with medium electron-dense granular content (Figure 6e).
在 . bicirrhosum 的 PGpn 卵母细胞内，线粒体开始分散在整个电子半透明卵原细胞体积内，但ER 形成了一个网络，位于细胞核附近（图 6c、d）。在卵质中，还存在大量溶酶体样体，可见圆形片状结构，含有中等电子密度的颗粒（图 6e）。

In A. gigas, PGpn oocytes ( filled with electron translucent ooplasm still contained a group of mitochondria with the germ plasm situated between them, whereas other organelles were dispersed. Cortical alveoli increased in number in different oocyte areas (Figure 6f).
在千足虫中，PGpn 卵母细胞 ( ，充满电子半透明卵浆，仍含有一组线粒体，种质位于线粒体之间，而其他细胞器则分散开来。皮质泡在不同卵母细胞区域的数量有所增加（图 6f）。

In all three studied species, we observed oocytes with peripherally arranged round cortical alveoli visible near oolemma and microvilli (Figure 7a-c). In P. buchholzi, these oocytes (119.76 were filled with electron translucent ooplasm only, and each contained one spherical anastomosing "net-like" structure formed by the germ plasm, which can be seen within the mitochondrial net (Figure 7D). Next, this structure dispersed throughout the ooplasm. In the oocytes of O. bicirrhosum and A. gigas , organelles were dispersed in the entire volume of the electron translucent ooplasm (Figure 7e,f).
在所研究的三个物种中，我们都观察到卵母细胞在卵膜和微绒毛附近可见外周排列的圆形皮质泡（图 7a-c）。在 P. buchholzi 中，这些卵母细胞（119.76 ）只充满了电子半透明卵质，每个卵母细胞都包含一个由胚芽质形成的球形吻合 "网状 "结构，可以在线粒体网内看到该结构（图 7d）。接下来，这种结构分散到整个卵原细胞中。在 O. bicirrhosum 和 A. gigas 的卵母细胞中，细胞器分散在整个电子半透明卵质中（图 7e,f）。

The Balbiani body, or its homolog, the Balbiani cytoplasm (Żelazowska et al., 2007), seems highly conservative because it appears in the oocytes of all vertebrates. However, in our study, we showed a significant diversity in Balbiani body organization during oogenesis in the three osteoglossiform species, both those internally and externally fertilizing.
Balbiani 体或其同源物 Balbiani 胞质（Żelazowska 等，2007 年）似乎非常保守，因为它出现在所有脊椎动物的卵母细胞中。然而，在我们的研究中，我们发现在三个骨舌形目物种的卵子发生过程中，Balbiani 体的组织结构具有显著的多样性，无论是内部受精还是外部受精。

FIGURE 7 Ultrastructure of parts of the early cortical alveoli oocytes of Pantodon buchholzi (a, d), Osteoglossum bicirrhosum (b, e), and Arapaima gigas (c, f). (a-c) Fragments of the perimetric ooplasm of the oocytes with peripherally arranged cortical alveoli. (d) Anastomosing "netlike" accumulations of the germ plasm forming round structure. (inset) The mitochondrion seen within the germ plasm. (e) Fragment of the ooplasm with dispersed mitochondria, endoplasmic reticulum, and lysosome-like bodies. (f) Fragment of the ooplasm with dispersed mitochondria and endoplasmic reticulum. CA, cortical alveolus; ER, endoplasmic reticulum; FC, follicular cell; GP, germ plasm; LB, lysosome-like body; M, mitochondrion; Mv, microvilli; , nucleus; , nucleolus; ZP, zona pellucida
图 7 Pantodon buchholzi（a，d）、Osteoglossum bicirrhosum（b，e）和 Arapaima gigas（c，f）早期皮质泡卵母细胞的部分超微结构。(a-c）卵母细胞周围的卵质片段，其外围排列着皮质泡。 d）吻合的 "网状 "种质堆积形成圆形结构。(插图）胚芽质中的线粒体。(e）带有分散线粒体、内质网和溶酶体样体的胚层碎片。(f）具有分散线粒体和内质网的卵原细胞片段。CA，皮质泡；ER，内质网；FC，滤泡细胞；GP，生殖质；LB，溶酶体样体；M，线粒体；Mv，微绒毛； ，细胞核； ，核仁；ZP，透明带。

TABLE 1 Different features of Balbiani body formation in Pantodon buchholzi, Osteoglossum bicirrhosum, and Arapaima gigas
表 1 Pantodon buchholzi、Osteoglossum bicirrhosum 和 Arapaima gigas 的 Balbiani 体形成的不同特征

In the osteoglossiforms studied here, as in other animals, such as the insect Thermobia domestica, zebrafish D. rerio, African clawed frog X. laevis, goat Capra bircus, and house mouse Mus musculus (Elkouby et al., 2016; Kloc et al., 2001, 2008; Kloc et al., 2004; Kloc et al., 2014; Kloc & Etkin, 2005; Marlow & Mullins, 2008), the process of Balbiani body formation is also reflected by polarization and
在本文研究的骨舌动物中，还有其他动物，如昆虫驯化瘤牛、斑马鱼、非洲爪蛙、山羊和家鼠（Elkouby 等，2016 年；Kloc 等，2001 年，2008 年；Kloc 等，2004 年；Kloc 等，2014 年；Kloc 和 Etkin，2005 年；Marlow 和 Mullins，2008 年）、2016; Kloc et al., 2001, 2008; Kloc et al., 2004; Kloc et al., 2014; Kloc & Etkin, 2005; Marlow & Mullins, 2008）。
asymmetry of the previtellogenic oocytes. In all described species and also in the three osteoglossiforms studied here, the Balbiani body was always enriched in the germ plasm, mitochondria, ER and Golgi apparatus (Kloc & Etkin, 2005; Żelazowska et al., 2007). However, the formation of some structures varied among studied species (Table 1 , Figures 8-11).
前细胞生成卵母细胞的不对称性。在所有已描述的物种中，以及在本文研究的三种骨舌虫中，巴尔比亚尼体总是富含种质、线粒体、ER 和高尔基体（Kloc 和 Etkin，2005 年；Żelazowska 等人，2007 年）。不过，所研究物种的某些结构的形成情况有所不同（表 1，图 8-11）。

In all studied osteoglossiforms, mitochondria were unevenly distributed within the ooplasm at the beginning of oogenesis. Subsequently, they formed a cluster and then fused into the mitochondrial network, which finally dispersed within the ooplasm (Figures 8-10). The variation of mitochondrial phenotype is a result of fusion and fission events (Chan, 2006). Skulachev (2001) suggested that fused mitochondria could allow a quick transmission of membrane potential to great distances in the cell, whereas fission of these organelles might favor recruitment of mitochondria into given compartments of the cell requiring adenosine triphosphate (ATP). Recent studies indicated that mitochondrial fission contributes to the induction of programmed cell death, while fusion has a protective role in this process (Olichon et al., 2003; Perfettini et al., 2005; Sugioka et al., 2004; Youle & Karbowski, 2005). In some bony fish, such as A. gueldenstaedtii, Polyodon spathula, and Acipenser baerii, two morphological types of mitochondria were described, with well-developed cristae and with
在所有研究的大骨节虫中，线粒体在卵子发生初期都不均匀地分布在卵质中。随后，它们形成一个线粒体集群，然后融合成线粒体网络，最后分散在卵质中（图 8-10）。线粒体表型的变化是融合和裂变事件的结果（Chan，2006 年）。斯库拉切夫（2001 年）认为，融合的线粒体可以将膜电位快速传递到细胞内的远处，而这些细胞器的裂变则可能有利于将线粒体招募到细胞内需要三磷酸腺苷（ATP）的特定区域。最近的研究表明，线粒体裂变有助于诱导细胞程序性死亡，而融合则在这一过程中起到保护作用（Olichon 等人，2003 年；Perfettini 等人，2005 年；Sugioka 等人，2004 年；Youle & Karbowski，2005 年）。在一些硬骨鱼（如 A. gueldenstaedtii、Polyodon spathula 和 Acipenser baerii）中，描述了两种形态的线粒体，一种是嵴发达的线粒体，另一种是嵴不发达的线粒体。

FIGURE 8 Changes in oocyte organization during early oogenesis in Pantodon buchholzi. In primary and secondary oogonia (OG I-II) as well as in early chromatin-nucleolus oocytes (leptotene, zygotene, pachytene), mitochondria, the endoplasmic reticulum, and the Golgi apparatus are evenly distributed within highly electron-dense ooplasm. Starting with the zygotene step, peripherally located nuclear material, a precursor of the germ plasm, is seen in the nucleus. In one-nucleolus oocyte (PGon), mitochondria and the endoplasmic reticulum begin to surround the nucleus. Early multiple-nucleoli oocyte (PGmn early) is filled with three types of ooplasm (highly electron-dense, medium electron-dense, and electron translucent). The nucleus and medium electron-dense ooplasm are surrounded by mitochondria scattered among the accumulation of the endoplasmic reticulum. In the late multiple-nucleoli oocyte (PGmn late), the volume of electron translucent ooplasm increases and the germ plasm is observed in close contact with mitochondria in highly electron-dense ooplasm and as round accumulations in medium electron-dense ooplasm. On the other hand, in the perinucleolar oocyte (PGpn), mitochondria form numerous independent clusters joined by the germ plasm. In medium electron-dense ooplasm, the germ plasm forms numerous "net-like" structures. At the beginning of the cortical alveolar step (PGca I), the oocyte contains one spherical anastomosing "net-like" structure formed by the germ plasm, visible within the mitochondrial net. Then (PGca II), this structure disperses throughout electron translucent ooplasm
图 8 Pantodon buchholzi 早期卵子发生过程中卵母细胞组织的变化。在初级和次级卵原细胞（OG I-II）以及早期染色质核仁卵母细胞（瘦卵母细胞、齐卵母细胞、厚卵母细胞）中，线粒体、内质网和高尔基体均匀地分布在电子密度很高的卵原细胞中。从合子期开始，细胞核中会出现位于外围的核物质，这是胚芽质的前身。在单核卵母细胞（PGon）中，线粒体和内质网开始包围细胞核。早期多核卵母细胞（PGmn early）充满了三种类型的卵质（高电子密度、中等电子密度和电子半透明）。细胞核和中等电子密度的卵原细胞被线粒体包围，线粒体散布在内质网的堆积物中。在晚期多核卵母细胞（PGmn late）中，电子半透明卵原细胞体积增大，在高电子密度卵原细胞中可观察到胚芽质与线粒体紧密接触，在中等电子密度卵原细胞中可观察到圆形堆积。另一方面，在核周卵母细胞（PGpn）中，线粒体形成许多独立的线粒体团，与胚芽质相连。在中等电子密度的卵原细胞中，胚芽质形成许多 "网状 "结构。在皮质肺泡步骤（PGca I）开始时，卵母细胞包含一个由胚芽质形成的球形吻合 "网状 "结构，在线粒体网中清晰可见。然后（PGca II），该结构分散到整个电子半透明卵质中

FIGURE 9 Changes in oocyte organization during early oogenesis in Osteoglossum bicirrhosum. In primary and secondary oogonia (OG I-II), mitochondria, the endoplasmic reticulum, and Golgi apparatus are evenly distributed within the ooplasm, where annulate lamellae appear during leptotene. In zygotene and pachytene oocytes, the nucleus comprises peripherally located nuclear material, whereas in the ooplasm, the Golgi apparatus forms complexes and the germ plasm is surrounded by mitochondria. In one-nucleolus oocyte (PGon), annulate lamellae disappear while the Golgi apparatus disperses within the ooplasm. The multiple-nucleoli oocyte ( ) is characterized by mitochondria interconnected into mitochondrial networks. These mitochondrial networks are joined with the germ plasm, which forms strings. The ooplasm of perinucleolar oocytes ( ) comprises numerous lysosome-like bodies, dispersed mitochondria, and endoplasmic reticulum network. At the beginning of the cortical alveolar step (PGca), all organelles are dispersed within the ooplasm
图 9 双脊龙虾早期卵子发生过程中卵母细胞组织的变化。在初级和次级卵原细胞（OG I-II）中，线粒体、内质网和高尔基体均匀地分布在卵原细胞内，其中环状薄片在瘦胚期出现。在合子期和长子期卵母细胞中，细胞核由位于外围的核物质组成，而在卵原质中，高尔基体形成复合体，胚质被线粒体包围。在单核卵母细胞（PGon）中，环状薄片消失，而高尔基体分散在卵质中。多核卵母细胞（ ）的特点是线粒体相互连接成线粒体网络。这些线粒体网络与种质相连，形成串状。核周卵母细胞（ ）的卵质由大量溶酶体样体、分散的线粒体和内质网组成。在皮层肺泡步骤（PGca）开始时，所有细胞器都分散在卵原质中

distorted cristae, which suggests degeneration of these organelles (Chan, 2006; Mishra & Chan, 2014; Żelazowska & Kilarski, 2009). This phenomenon could support the hypothesis of the selection of mitochondria that would be passed on to the future embryo (Tworzydlo et al., 2020).
嵴扭曲，这表明这些细胞器发生了退化（Chan，2006 年；Mishra & Chan，2014 年；Żelazowska & Kilarski，2009 年）。这一现象可以支持选择线粒体遗传给未来胚胎的假设（Tworzydlo 等人，2020 年）。

The ER, which is the largest and one of the most morphologically variable membranous organelles (Borgese et al., 2006; Snapp, 2005), is observed in the oocytes of all three studied osteoglossiform species, both in dispersed and differentiated forms (as mitochondriaassociated membranes, annulate lamellae, network of tubules, karmellae, and whorls; Figures 8-10). Additionally, in P. buchholzi, the ER and mitochondria together form a cluster during the multiple nucleoli step. A link between these two types of organelles, including close appositions and communication between them, is referred to as mitochondria-associated membranes (Vance, 1990). It was described in several cell types and is involved mainly in lipid transfer and exchanging ions between mitochondria and the ER (Giorgi et al., 2009).
ER是最大的膜状细胞器，也是形态变化最大的膜状细胞器之一（Borgese等人，2006年；Snapp，2005年），在所研究的三个骨舌鱼种的卵母细胞中均可观察到ER，既有分散形态，也有分化形态（线粒体相关膜、环状薄片、管状网络、脐状膜和轮状膜；图8-10）。此外，在 P. buchholzi 中，ER 和线粒体在多核小体步骤中共同形成一个簇。这两种细胞器之间的联系，包括它们之间的紧密结合和交流，被称为线粒体相关膜（Vance，1990 年）。它在几种细胞类型中都有描述，主要参与线粒体和 ER 之间的脂质转移和 离子交换（Giorgi 等人，2009 年）。

The annulate lamellae were present only in . bicirrhosum. These ooplasmic organelles consist of membrane cisternae of the ER with pore complexes similar to nuclear pore complexes (Kessel, 1992; Snapp, 2005). They are often continuous with the nuclear envelope and ER (Kessel, 1989, 1992). Annulate lamellae have been observed in different cells, but often in cancer cells and in the oocytes of several species across the whole animal kingdom: the fruit fly . melanogaster, dragonfly Libellula pulchella, snail Otala lactea, surf clam Spisula solidissima, African clawed frog X. laevis, newt Triturus viridescens, and even in humans (Dabauvalle et al., 1991; Hertig, 1968; Kessel & Beams, 1969; Okada & Waddington, 1959; Swift, 1956; Wischnitzer, 1960). Their functions are poorly understood, although it was postulated that annulate lamellae in mammals can influence the rates of nuclear import and export (Raghunayakula et al., 2015).
环状薄片只出现在 . bicirrhosum 中。这些质细胞器由具有与核孔复合体类似的孔复合体的 ER 膜腔组成（Kessel，1992 年；Snapp，2005 年）。它们通常与核包膜和 ER 相连（Kessel，1989 年，1992 年）。在不同的细胞中都观察到了环状薄片，但通常是在癌细胞和整个动物界的一些物种的卵母细胞中：果蝇 . melanogaster、蜻蜓 Libellula pulchella、蜗牛 Otala lactea、海蚌 Spisula solidissima、非洲爪蛙 X. laevis、蝾螈 Triturus viridescens，甚至在人体内也观察到了环状薄片（Dabauvalle 等人，1991 年；Hertig，1968 年）、1991；Hertig，1968；Kessel & Beams，1969；Okada & Waddington，1959；Swift，1956；Wischnitzer，1960）。尽管有人推测哺乳动物的环状薄片可以影响核输入和输出的速率，但对它们的功能却知之甚少（Raghunayakula 等人，2015 年）。

In the perinucleolar oocytes of . bicirrhosum, the ER forms a network. This is a rapid process consisting of two steps: fusion of the membranes and formation of the network (Snapp, 2005). An ATP-dependent -ethylmaleimide sensitive fusion protein (NSF), vand t-SNAREs, receptor proteins, and possibly a Rab protein are involved in the first step (Chen & Scheller, 2001; Latterich & Patel, 1998; Malhotra et al., 1988; Pelham, 2001; Zerial & McBride, 2001), whereas energy (ATP and GTP), microtubules, and microtubule-associated motor proteins are required for the second step (Dabora & Sheetz, 1988; Lane & Allan, 1999; Vale & Hotani, 1988).
在 . bicirrhosum 的核周卵母细胞中，ER 形成了一个网络。这是一个快速过程，包括两个步骤：膜的融合和网络的形成（Snapp，2005 年）。依赖于 ATP 的 -乙基马来酰亚胺敏感融合蛋白（NSF）、v 和 t-SNARE、受体蛋白以及可能的 Rab 蛋白参与了第一步（Chen & Scheller, 2001; Latterich & Patel, 1998; Malhotra et al、1988；Pelham，2001；Zerial & McBride，2001），而第二步则需要能量（ATP 和 GTP）、微管和微管相关运动蛋白（Dabora & Sheetz，1988；Lane & Allan，1999；Vale & Hotani，1988）。

In the oogonia of A. gigas, karmellae and whorls are present. They are formed by the smooth ER and may be present in the same cell (Snapp, 2005), as in A. gigas. This phenomenon suggests that these structures may be different stages of organized smooth ER (Snapp, 2005).
在千头椿的卵原细胞中，存在着卡氏体和轮纹。它们由光滑 ER 形成，可能存在于同一个细胞中（Snapp，2005 年），千足虫也是如此。这一现象表明，这些结构可能是有组织的光滑 ER 的不同阶段（Snapp，2005 年）。

During oogenesis, we noted a sequence of germ plasm accumulations (Figure 11), partly similar to those described in Xiphophorus helleri by Azevedo (1984). The germ plasm is formed just under the nuclear envelope after passing through the nuclear envelope as small aggregations of electron-dense material as in . buchholzi,
在卵子发生过程中，我们注意到了胚芽质积累的序列（图 11），部分类似于 Azevedo（1984 年）在 Xiphophorus helleri 中描述的序列。与 . buchholzi 中的情况一样，种质以电子致密物质的小聚合体形式穿过核膜后在核膜下形成、

FIGURE 10 Changes in oocyte organization during early oogenesis in Arapaima gigas. In primary oogonia (OG I), mitochondria, the endoplasmic reticulum, and Golgi apparatus are evenly distributed within the ooplasm. Secondary oogonia (OG II) contain also karmellae and whorls, which are absent in leptotene oocytes. During zygotene, some alveoli appear in the ooplasm. In early pachytene oocytes, irregularly shaped nuclear material passes through the nuclear envelope. In the ooplasm, mitochondria form a cluster surrounded by the endoplasmic reticulum. During late pachytene, assembly of the germ plasm formed by peripherally located highly electron-dense material, which surrounds medium electron-dense material, is observed in close contact with mitochondria. In one-nucleolus oocyte (PGon), numerous accumulations of the germ plasm are present within mitochondria that still form a cluster. In multiple nucleoli (PGmn) and perinuleolar (PGpn) oocytes, the mitochondrial net is formed by fusion of mitochondria. In cortical alveoli oocytes (PGca), all organelles are dispersed
图 10 巨嘴鸟早期卵子发生过程中卵母细胞组织的变化。在初级卵原细胞（OG I）中，线粒体、内质网和高尔基体均匀地分布在卵原细胞中。次级卵原细胞（OG II）中还含有脐带和轮纹，而在瘦卵母细胞中则没有。在合子期，卵原细胞中出现了一些肺泡。在早期卵母细胞中，形状不规则的核物质穿过核膜。在卵原质中，线粒体形成一个由内质网包围的团块。在萌发后期，可观察到由位于外围的高电子密度物质形成的胚质与线粒体紧密接触，而胚质则围绕着中等电子密度物质。在单核卵母细胞（PGon）中，线粒体内有大量胚芽质堆积，这些胚芽质仍形成一个簇。在多核卵母细胞（PGmn）和小叶周围卵母细胞（PGpn）中，线粒体网由线粒体融合形成。在皮质肺泡卵母细胞（PGca）中，所有细胞器都是分散的
O. bicirrhosum (this study) and many other fish species (Grier, 2000, 2012; Żelazowska et al., 2007; Żelazowska & Fopp-Bayat, 2019; Żelazowska & Halajian, 2019; Żelazowska & Kilarski, 2009) or as irregularly shaped electron-dense material, which was observed in A. gigas (this study) and in X. helleri (Azevedo, 1984). Germ plasm accumulations are visible in ooplasm in close contact with mitochondria. This phenomenon was often described in the oocytes of various species (Azevedo, 1984; Grier, 2000, 2012; Żelazowska et al., 2007; Żelazowska & Fopp-Bayat, 2019; Żelazowska & Halajian, 2019; Żelazowska & Kilarski, 2009). In all three studied osteoglossiforms, the germ plasm is present between mitochondria within the mitochondrial network. The anastomosing "net-like" structure formed by the germ plasm present in . buchholzi seems to be similar to round bodies described in the oocytes of some teleosts, for example, in antarctic notothenioids (nototheniids and channichthyids) and in temperate Salmo gairdneri. Oryzias latipes, and O. mykiss (Beams & Kessel, 1973, 1974; Fusco et al., 2000; Hamaguchi, 1985; Kobayashi & Iwamatsu, 2000; Motta et al., 2005). Among notothenioids, there is a variation in terms of the presence, number, and size of the round bodies, which are visible as "a regular arrangement of finely granular, dense cords surrounded by a halo of short fibrillae" (Motta et al., 2005) and contain rRNA. Nototheniids (Trematomus bernacchii, T. hansoni, T. pennelli, T. lepidorhinus, Pagothenia borkgrevinki) possess large round bodies (up to ), while in channichthyids (Pagetopsis macropterus, Chionodraco hamatus, Cryodraco antarticus), the round bodies are smaller (less than ) and more numerous (3-4 per oocyte). In contrast, Gymnodraco acuticeps, a representative of bathydraconids, does not have the round bodies (Motta et al., 2005). Fusco et al. (2000), in their detailed analysis of the round bodies in the salmonid 0 . mykiss, indicated that in the early primary growth stage, 2 to 6 small round bodies are dispersed in the perinuclear region of the ooplasm, whereas in larger oocytes only one or two peripherally arranged bigger bodies ( ) are present. Each round body consists of "tridimensional net" of "cords forming polygonal grids" and some small mitochondria and vesicles between the net and contain proteins, nucleic acids, and rRNA. They hypothesized that the round bodies may "overcome the temporary stop of rRNA synthesis during the formation of multiple nucleoli” (Fusco et al., 2000).
本研究）和许多其他鱼类物种（Grier，2000 年，2012 年；Żelazowska 等人，2007 年；Żelazowska & Fopp-Bayat，2019 年；Żelazowska & Halajian，2019 年；Żelazowska & Kilarski，2009 年），或者是不规则形状的电子致密物质，这在千足类（本研究）和 X. helleri（Azevedo，1984 年）中都有观察到。在与线粒体密切接触的卵质体中可以看到胚芽质堆积。这种现象经常在不同物种的卵母细胞中出现（Azevedo，1984 年；Grier，2000 年，2012 年；Żelazowska 等人，2007 年；Żelazowska & Fopp-Bayat，2019 年；Żelazowska & Halajian，2019 年；Żelazowska & Kilarski，2009 年）。在研究的所有三种骨舌动物中，种质都存在于线粒体网络内的线粒体之间。 . buchholzi 中的种质形成的吻合 "网状 "结构似乎类似于一些远洋鱼类卵母细胞中的圆形体，例如南极蝾螈类（nototheniids 和 channichthyids）和温带 Salmo gairdneri。Oryzias latipes 和 O. mykiss（Beams 和 Kessel，1973 年，1974 年；Fusco 等人，2000 年；Hamaguchi，1985 年；Kobayashi 和 Iwamatsu，2000 年；Motta 等人，2005 年）。在蝾螈类动物中，圆形体的存在、数量和大小存在差异，可见 "细颗粒状的致密绳索规则排列，周围环绕着短纤维晕"（Motta 等人，2005 年），并含有 rRNA。Nototheniids （Trematomus bernacchii、T. hansoni、T. pennelli、T. lepidorhinus、Pagothenia borkgrevinki）拥有大的圆形体（高达 ），而在 channichthyids （Pagetopsis macropterus、Chionodraco hamatus、Cryodraco antarticus）中，圆形体较小 （小于 ），数量较多（每个卵母细胞 3-4 个）。与此相反，Gymnodraco acuticeps（浴栉水母的代表）没有圆形体（Motta 等人，2005 年）。Fusco 等人（2000 年）对鲑科鱼类 0. mykiss 的圆体进行了详细分析，结果表明，在初级生长阶段的早期，2 到 6 个小 圆体分散在卵母细胞的核周区域，而在较大的卵母细胞中，只有一个或两个外围排列的较大的圆体 ( ) 存在。每个圆体由 "形成多边形网格的绳索 "的 "三维网 "和网间的一些小线粒体和囊泡组成，含有蛋白质、核酸和 rRNA。他们推测，圆形体可能 "克服了多个核小体形成过程中 rRNA 合成暂时停止的问题"（Fusco 等人，2000 年）。

In our study, O. bicirrhosum was the only species with a complex Golgi apparatus located close to each other in the form of a cluster. The Golgi apparatus is involved in processing and sorting proteins and lipids moving through the secretory pathway (Pepling et al., 2007; Sengupta & Linstedt, 2011). As previously shown, variations in the shape and size of the complexes of Golgi apparatus are correlated with their dynamics and function in different cell types (Kreft et al., 2010; Lu et al., 2001; Rao et al., 2018; Watanabe et al., 2012).
在我们的研究中，O. bicirrhosum 是唯一一个具有复杂高尔基体的物种，这些高尔基体以簇的形式相互靠近。高尔基体参与处理和分类通过分泌途径移动的蛋白质和脂质（Pepling 等人，2007 年；Sengupta & Linstedt，2011 年）。如前所述，高尔基体复合物形状和大小的变化与其在不同细胞类型中的动态和功能相关（Kreft 等人，2010 年；Lu 等人，2001 年；Rao 等人，2018 年；Watanabe 等人，2012 年）。

FIGURE 11 Differences in the formation of the germ plasm during early oogenesis in Pantodon buchholzi (left column), Osteoglossum bicirrhosum (middle column), and Arapaima gigas (right column). P. buchholzi: (1) Nuclear material is peripherally located within the nucleus, whereas in highly electron-dense ooplasm, the germ plasm is seen both close to the nuclear envelope or surrounded by mitochondria. In medium electron-dense ooplasm, the germ plasm is visible as round accumulations. (2) The germ plasm is still surrounded by mitochondria in highly electron-dense ooplasm, whereas in medium electron-dense ooplasm, it forms numerous "net-like" structures. (3) Mitochondria surrounding the germ plasm become more numerous, whereas the "net-like" structures increase their dimensions. (4) Fused mitochondria and one great "net-like" germ plasm form a round structure present in electron translucent ooplasm. O. bicirrhosum: (1) Nuclear material is peripherally located within the nucleus, whereas in the ooplasm, the germ plasm is seen close to the nuclear envelope or mitochondria. (2) Numerous mitochondria surround accumulations of the germ plasm. (3) These structures are seen closer to each other. (4) Fused mitochondria are joined with the germ plasm that forms strings. A. gigas: (1) Irregularly shaped nuclear material passes through the nuclear envelope, whereas in ooplasm, mitochondria form a cluster. (2) The germ plasm is observed in close contact with mitochondria. The germ plasm is formed by peripherally located highly electrondense material (black), which surrounds medium electron-dense material (gray). (3) Numerous accumulations of the germ plasm are seen within mitochondria that still form a cluster. (4) Fused mitochondria are interconnected by accumulations of the germ plasm. GP, germ plasm; M, mitochondrion; N, nucleus; NE, nuclear envelope; Nuclear material; I, highly electron-dense ooplasm; II, medium electron-dense ooplasm; III, electron translucent ooplasm
图 11 Pantodon buchholzi（左侧一栏）、Osteoglossum bicirrhosum（中间一栏）和 Arapaima gigas（右侧一栏）早期卵子发生过程中胚质形成的差异。P. buchholzi：(1) 核物质位于细胞核的外围，而在高电子密度的卵质中，生殖质紧贴核膜或被线粒体包围。在中等电子密度的细胞质中，胚芽质呈圆形堆积。(2）在高电子密度的卵原细胞中，胚芽质仍被线粒体包围，而在中等电子密度的卵原细胞中，胚芽质则形成许多 "网状 "结构。(3) 种质周围的线粒体数量增加，而 "网状 "结构的尺寸增大。(4）融合的线粒体和一个巨大的 "网状 "种质形成一个圆形结构，存在于电子半透明的卵质中。O. bicirrhosum：（1）核物质位于细胞核的外围，而在细胞质中，胚芽质靠近核膜或线粒体。(2）大量线粒体围绕着胚芽质的堆积。(3) 这些结构彼此更接近。(4)融合的线粒体与种质结合成串。千足虫：（1）形状不规则的核物质穿过核包膜，而在卵质中，线粒体形成一个簇。(2）胚芽质与线粒体紧密接触。胚芽质由位于外围的高电子密度物质（黑色）构成，其周围是中等电子密度物质（灰色）。(3) 线粒体内可见大量胚芽质堆积，但仍形成一个线粒体簇。(4)融合的线粒体通过胚芽质的堆积相互连接。GP，胚芽质；M，线粒体；N，细胞核；NE，核膜；核材料；I，高度电子致密的细胞质；II，中等电子致密的细胞质；III，电子半透明的细胞质。

This especially characterizes oocytes during their development (Ikami et al., 2017; Moreno et al., 2002).
这尤其是卵母细胞在发育过程中的特征（Ikami 等人，2017 年；Moreno 等人，2002 年）。

In addition, in . bicirrhosum small spherical lamellar structures with granular content were present in the ooplasm, increasing in number with oogenesis progression. They seem to be similar to lysosomelike bodies described by Żelazowska and Halajian (2019) in the oocytes of M. salmoides. However, their function is still unknown.
此外，在 . bicirrhosum 中，卵质中存在颗粒状的小球形片状结构，其数量随着卵子发生的进展而增加。它们似乎类似于Żelazowska 和 Halajian（2019 年）在鲑鱼卵母细胞中描述的溶酶体。然而，它们的功能仍然未知。

During all steps of previtellogenesis, the oocytes of . bicirrhosum and A. gigas were filled with electron translucent ooplasm. However, in P. buchholzi, we observed three types of ooplasm with different electron density: highly electron-dense ooplasm that filled the earliest oocytes; subsequently, medium electron-dense ooplasm, containing the germ plasm, which formed close to the nucleus and then dispersed; and electron translucent ooplasm that significantly increased and finally entirely replaced highly electron-dense ooplasm. Żelazowska et al. (2007) described zonation of the ooplasm filing the previtellogenic oocytes of . gueldenstaedtii. Only the centrally located zone of the ooplasm, named Balbiani cytoplasm, contained components of the Balbiani body (but formation of the Balbiani body was not observed), whereas peripheral zone was organelle free. In
在前细胞发生的所有阶段， . bicirrhosum 和千足虫的卵母细胞都充满了电子半透明的卵原细胞。但在布氏袋鲤中，我们观察到了三种不同电子密度的卵原细胞：高电子密度卵原细胞充满了最早的卵母细胞；随后是中等电子密度卵原细胞，其中包含种质，靠近细胞核形成，然后分散；电子半透明卵原细胞显著增加，最后完全取代了高电子密度卵原细胞。Żelazowska 等人（2007 年）描述了 . gueldenstaedtii 的前细胞发生卵母细胞中的卵原细胞分区。只有位于中央的卵原质区（名为 Balbiani 细胞质）含有 Balbiani 体的成分（但未观察到 Balbiani 体的形成），而外围区则不含细胞器。在

P. buchholzi, we do not define the Balbiani cytoplasm, because in this species the Balbiani body is formed regardless of the formation of the three ooplasm zones.
我们没有定义巴尔比亚尼细胞质，因为在该物种中，无论是否形成三个细胞质区，都会形成巴尔比亚尼体。

The general characteristics of Balbiani body development shows some similarities between . buchholzi, O. bicirhosum, and A. gigas as well as other previously described species. Moreover, these features seem to be highly conservative (asymmetry of the oocyte, presence of the germ plasm, fusion and fission of mitochondria). However, there are some peculiar characteristics for each of the studied species, including the three types of ooplasm with different electron density in P. buchholzi; annulate lamellae, complexes of Golgi apparatus, ER network, and multiple lysosome-like bodies in O. bicirrhosum; and, finally, karmellae and whorls as well as irregularly shaped nuclear material that passes through the nuclear envelope in A. gigas. The internally fertilizing . buchholzi, which is probably the most basal osteoglossiform, possesses unique state of ooplasm being electron dense at the beginning of oogenesis and seems to have numerous features in Balbiani body formation.
Balbiani 身体发育的一般特征与 . buchholzi、O. bicirhosum 和 A. gigas 以及之前描述的其他物种有一些相似之处。此外，这些特征似乎非常保守（卵母细胞不对称、种质的存在、线粒体的融合和分裂）。不过，所研究的每个物种都有一些特殊的特征，包括布氏栉水母（P. buchholzi）具有电子密度不同的三种卵原细胞；双鳃水母（O. bicirrhosum）具有环状薄片、高尔基体复合体、ER 网络和多个溶酶体样体；最后，千足金枪鱼（A. gigas）具有脐带和轮纹以及穿过核膜的不规则形状的核物质。内部受精的 . buchholzi 可能是最基干的骨舌体，在卵子发生初期具有独特的电子致密的卵质状态，似乎具有许多 Balbiani 体形成的特征。

Existing data about ultrastructure of the Balbiani body are scarce and mostly refer to more derived species of bony fish with external fertilization (Azevedo, 1984; Beams & Kessel, 1973, 1974; Fusco et al., 2000; Grier, 2000, 2012; Hamaguchi, 1985; Kobayashi & Iwamatsu, 2000; Motta et al., 2005; Żelazowska et al., 2007; Żelazowska & Fopp-Bayat, 2019; Żelazowska & Halajian, 2019; Żelazowska & Kilarski, 2009). Therefore, future studies should investigate if the reproductive mode, which is highly associated with sperm structure, is also correlated with oocyte development and its final structure. The diversity of structures forming the Balbiani body in osteoglossiforms indicates that the variety of gamete structure in this group, which has been described so far only for spermatogenesis and spermatozoa (Mattei, 1970, 1991; Mattei et al., 1967; Mattei et al., 1972; Mattei et al., 2019; van Deurs, 1973; van Deurs & Lastein, 1973), is visible also in the organization of the ooplasm in oocytes. The phylogenetic divergence about 150 Mya of lineages of Pantodontidae and Osteoglossidae as well as about 110 Mya of subfamilies of Osteoglossidae might have been a reason of variability in the Balbiani body in three studied species. Therefore, future research on reproductive biology as well as other aspects of Osteoglossomorpha, one of the most basal Teleostei group, can provide new insight into the long-lasting evolution of fish.
关于巴尔比亚尼体超微结构的现有数据很少，而且大多是关于具有体外受精功能的骨鱼的衍生物种（Azevedo，1984；Beams & Kessel，1973，1974；Fusco 等，2000；Grier，2000，2012；Hamaguchi，1985；Kobayashi & Iwamatsu，2000；Motta 等，2005；Żelazowska 等、2000；Grier，2000，2012；Hamaguchi，1985；Kobayashi & Iwamatsu，2000；Motta 等人，2005；Żelazowska 等人，2007；Żelazowska & Fopp-Bayat，2019；Żelazowska & Halajian，2019；Żelazowska & Kilarski，2009）。因此，未来的研究应该调查与精子结构高度相关的繁殖模式是否也与卵母细胞的发育及其最终结构相关。骨舌虫巴尔比亚尼体结构的多样性表明，该类群配子结构的多样性迄今仅在精子发生和精子方面有所描述（Mattei，1970 年，1991 年；Mattei 等人，1967 年；Mattei 等人，1972 年；Mattei 等人，2019 年；van Deurs，1973 年；van Deurs & Lastein，1973 年），在卵母细胞的卵质组织中也是可见的。Pantodontidae和Osteoglossidae各系约150 Mya的系统发育分化，以及Osteoglossidae亚科约110 Mya的系统发育分化，可能是造成所研究的三个物种Balbiani体变异的原因。因此，未来对最基底的长目鱼类之一的骨舌鱼科的生殖生物学及其他方面的研究，可以为鱼类的长期进化提供新的见解。

The authors are grateful to Dr D. Podkowa (Department of Comparative Anatomy) and Dr O. Woźnicka (Department of Cell Biology and Imaging) for technical facilities in transmission electron microscopy; and to the Department of Cell Biology and Imaging, Institute of Zoology and Biomedical Research, Jagiellonian University. The work was supported by Jagiellonian University funds (N18/DBS/000005; to Anna Pecio and Rafal P. Piprek), (K/DSC/005532; to Anna M. Dymek) and funds of PhD Students Society of Jagiellonian University in Krakow for Anna M. Dymek.
作者感谢 D. Podkowa 博士（比较解剖学系）和 O. Woźnicka 博士（细胞生物学和成像学系）提供的透射电子显微镜技术设施，并感谢雅盖隆大学动物学和生物医学研究所细胞生物学和成像学系。安娜-佩西奥（Anna Pecio）和拉法尔-皮普雷克（Rafal P. Piprek）的研究经费（K/DSC/005532；安娜-戴梅克（Anna M. Dymek）的研究经费）以及克拉科夫雅盖隆大学博士生协会为安娜-戴梅克（Anna M. Dymek）提供的经费。

The authors declare no potential conflict of interest.
作者声明没有潜在的利益冲突。

Anna Dymek: Conceptualization; investigation; methodology; resources; visualization; writing-original draft; writing-review & editing. Anna Pecio: Conceptualization; methodology; visualization; writing-original draft; writing-review & editing. Rafal Piprek: Conceptualization; writing-original draft; writing-review editing.
安娜-戴梅克概念化；调查；方法；资源；可视化；写作-原稿；写作-审阅和编辑。Anna Pecio：概念化；方法论；可视化；撰写-原稿；撰写-审阅和编辑。Rafal Piprek：概念化；撰写-原稿；撰写-审核 编辑。

The peer review history for this article is available at https://publons. com/publon/10.1002/jmor.21387.
本文的同行评审记录可在 https://publons. com/publon/10.1002/jmor.21387 上查阅。

The data that support the findings of this study are available from the corresponding author upon reasonable request.
支持本研究结果的数据可向相应作者索取。

Anna M. Dymek (D) https://orcid.org/0000-0002-0557-9619

Anna Pecio (D) https://orcid.org/0000-0001-9052-5844

Rafal P. Piprek (D) https://orcid.org/0000-0002-0018-2444

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How to cite this article: Dymek, A. M., Pecio, A., & Piprek, R. P. (2021). Diversity of Balbiani body formation in internally and externally fertilizing representatives of Osteoglossiformes (Teleostei: Osteoglossomorpha). Journal of Morphology, 282(9), 1313-1329. https://doi.org/10.1002/jmor. 21387
如何引用本文：Dymek, A. M., Pecio, A., & Piprek, R. P. (2021).骨舌形目（远洋鱼类：Osteoglossomorpha）体内和体外受精代表鱼类巴尔比亚尼体形成的多样性。形态学杂志》，282（9），1313-1329。https://doi.org/10.1002/jmor。21387