Background The vast majority of nematode species have vermiform (worm-shaped) body plans throughout post-embryonic development. However, atypical body shapes have evolved multiple times. The plant-parasitic Tylenchomorpha nematode Heterodera glycines hatches as a vermiform infective juvenile. Following infection and the establishment of a feeding site, H. glycines grows disproportionately greater in width than length, developing into a saccate adult. Body size in Caenorhabditis elegans was previously shown to correlate with post-embryonic divisions of laterally positioned stem cell-like 'seam' cells and endoreduplication of seam cell epidermal daughters. To test if a similar mechanism produces the unusual body shape of saccate parasitic nematodes, we compared seam cell development and epidermal ploidy levels of H. glycines to C. elegans. To study the evolution of body shape development, we examined seam cell development of four additional Tylenchomorpha species with vermiform or saccate body shapes. Results We confirmed the presence of seam cell homologs and their proliferation in H. glycines. This results in the adult female epidermis having approximately 1800 nuclei compared with the 139 nuclei in the primary epidermal syncytium of C. elegans. Similar to C. elegans, we found a significant correlation between H. glycines body volume and the number and ploidy level of epidermal nuclei. While we found that the seam cells also proliferate in the independently evolved saccate nematode Meloidogyne incognita following infection, the division pattern differed substantially from that seen in H. glycines. Interestingly, the close relative of H. glycines, Rotylenchulus reniformis does not undergo extensive seam cell proliferation during its development into a saccate form. Conclusions Our data reveal that seam cell proliferation and epidermal nuclear ploidy correlate with growth in H. glycines. Our finding of distinct seam cell division patterns in the independently evolved saccate species M. incognita and H. glycines is suggestive of parallel evolution of saccate forms. The lack of seam cell proliferation in R. reniformis demonstrates that seam cell proliferation and endoreduplication are not strictly required for increased body volume and atypical body shape. We speculate that R. reniformis may serve as an extant transitional model for the evolution of saccate body shape.

中文翻译：

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线虫中囊状体形的趋同进化通过不同的发育机制。

背景 绝大多数线虫物种在胚胎后发育过程中都具有蠕虫状（蠕虫状）体型。然而，非典型的体型已经进化了多次。植物寄生的 Tylenchomorpha 线虫 Heterodera glycines 孵化为蠕虫状感染幼虫。在感染和建立摄食位点后，H. glycines 的宽度比长度长得不成比例，发育成囊状成虫。先前显示秀丽隐杆线虫的体型与横向定位的干细胞样“接缝”细胞的胚胎后分裂和接缝细胞表皮子代的核内复制相关。为了测试类似的机制是否会产生囊状寄生线虫的异常体型，我们比较了 H. glycines 与 C. elegans 的接缝细胞发育和表皮倍性水平。为了研究体形发育的演变，我们检查了另外四种具有蠕虫状或囊状体形的 Tylenchomorpha 物种的接缝细胞发育。结果我们证实了在H.甘氨酸中存在接缝细胞同源物及其增殖。这导致成年雌性表皮具有大约 1800 个细胞核，而秀丽隐杆线虫的初级表皮合胞体中有 139 个细胞核。与 C. elegans 相似，我们发现 H. glycines 体体积与表皮细胞核的数量和倍性水平之间存在显着相关性。虽然我们发现接缝细胞也在感染后独立进化的囊状线虫南方根结线虫中增殖，但分裂模式与 H. glycines 中的分裂模式有很大不同。有趣的是，H. glycines 的近亲，Rotylenchurus reniformis 在其发展成囊状形式期间不经历广泛的接缝细胞增殖。结论 我们的数据表明，接缝细胞增殖和表皮核倍性与 H. glycines 的生长相关。我们在独立进化的囊状物种 M. incognita 和 H. glycines 中发现了不同的接缝细胞分裂模式，这表明囊状形式的平行进化。R. reniformis 中缺乏接缝细胞增殖表明，增加体体积和非典型体形并不严格要求接缝细胞增殖和核内复制。我们推测 R. reniformis 可能作为囊状体形进化的现存过渡模型。结论 我们的数据表明，接缝细胞增殖和表皮核倍性与 H. glycines 的生长相关。我们在独立进化的囊状物种 M. incognita 和 H. glycines 中发现了不同的接缝细胞分裂模式，这表明囊状形式的平行进化。R. reniformis 中缺乏接缝细胞增殖表明，增加体体积和非典型体形并不严格要求接缝细胞增殖和核内复制。我们推测 R. reniformis 可能作为囊状体形进化的现存过渡模型。结论 我们的数据表明，接缝细胞增殖和表皮核倍性与 H. glycines 的生长相关。我们在独立进化的囊状物种 M. incognita 和 H. glycines 中发现了不同的接缝细胞分裂模式，这表明囊状形式的平行进化。R. reniformis 中缺乏接缝细胞增殖表明，增加体体积和非典型体形并不严格要求接缝细胞增殖和核内复制。我们推测 R. reniformis 可能作为囊状体形进化的现存过渡模型。甘氨酸暗示囊状形式的平行进化。R. reniformis 中缺乏接缝细胞增殖表明，增加体体积和非典型体形并不严格要求接缝细胞增殖和核内复制。我们推测 R. reniformis 可能作为囊状体形进化的现存过渡模型。甘氨酸暗示囊状形式的平行进化。R. reniformis 中缺乏接缝细胞增殖表明，增加体体积和非典型体形并不严格要求接缝细胞增殖和核内复制。我们推测 R. reniformis 可能作为囊状体形进化的现存过渡模型。