Widespread presence of human BOULE homologs among animals and conservation of their ancient reproductive function.
Widespread presence of human BOULE homologs among animals and conservation of their ancient reproductive function.
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DOI：
10.1371/journal.pgen.1001022
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发表时间：
2010-07-15
期刊：
影响因子：
4.5
通讯作者：
Xu EY
中科院分区：
文献类型：
--
作者：
Shah C;Vangompel MJ;Naeem V;Chen Y;Lee T;Angeloni N;Wang Y;Xu EY
性别特异性特征导致产生二型配子，雄性的精子和雌性的卵子，是有性生殖的基础，因此在动物中广泛存在。然而，这些性别特异性特征背后的性别偏见基因处于强大的选择压力之下，并且由于适应性进化，它们经常变得不同。事实上，在不同生物体中发现的数百个雄性或雌性生育基因中，只有极少数与一个以上谱系的生殖有关。很少有基因表现出性别偏见，生殖特定的要求超出了一个给定的门，提出了一个问题，是否有任何性别特异性配子发生的因素可以被保存，配子发生是否可能已经进化了多次。在这里，我们描述了一个后生动物的起源保守的人类生殖蛋白，BOULE，和它的患病率从原始的基底后生动物脊索动物。我们发现，BOULE同源物存在于后生动物的每个主要谱系的代表性物种的基因组中，并表现出生殖特异性表达在所有物种的研究，男性偏见的表达占优势。对昆虫和哺乳动物谱系内的Boule进化的研究显示，与大多数生殖基因不同，几乎没有证据表明加速进化。相反，净化选择是波尔进化背后的主要力量。此外，哺乳动物Boule功能的丧失导致雄性特异性不育和精子发育的全面停滞，这与昆虫boule突变中的表型非常相似。这项工作表明，整个真后生动物的生殖蛋白的保护，其主要的睾丸偏见在不同的两侧体物种的表达，并在小鼠中的雄性配子发生的要求的保护。这表明了一个古老的配子发生的要求之间的Bilateria和支持精子发生的共同起源的模型。虽然有性生殖在动物中很普遍，但有性生殖在多大程度上是保守的，以及性别特异性配子发生（精子发生和卵子发生）何时起源于动物仍然是个谜。在这里，我们证明了生殖特异性蛋白质的存在下，整个双边对称的动物（Bilateria）和保护其男性生殖功能的小鼠。在昆虫和哺乳动物谱系中，代表双边动物的原口目和次口目分支的Boule进化的检查，没有发现任何加速进化的证据。相反，净化选择是波尔进化背后的主要力量。进一步调查的Boule同源物之间的Deuterostome物种发现生殖特异性表达，具有很强的患病率睾丸偏见的表达。我们通过在小鼠（一种代表性哺乳动物，一种后口动物）中灭活Boule进一步确定了后口动物Boule同源物的功能。与果蝇（原口门进化支的代表）的对应物一样，小鼠的卵珠也只在雄性生殖时需要。小鼠睾丸的缺失会阻止精子的产生，导致精子发生的全面停滞，这与果蝇睾丸突变体的情况非常相似。我们的研究结果是一致的雄性配子发生之间的后生动物的共同起源，并揭示了高保守性的生殖特异性蛋白质两侧动物。
Sex-specific traits that lead to the production of dimorphic gametes, sperm in males and eggs in females, are fundamental for sexual reproduction and accordingly widespread among animals. Yet the sex-biased genes that underlie these sex-specific traits are under strong selective pressure, and as a result of adaptive evolution they often become divergent. Indeed out of hundreds of male or female fertility genes identified in diverse organisms, only a very small number of them are implicated specifically in reproduction in more than one lineage. Few genes have exhibited a sex-biased, reproductive-specific requirement beyond a given phylum, raising the question of whether any sex-specific gametogenesis factors could be conserved and whether gametogenesis might have evolved multiple times. Here we describe a metazoan origin of a conserved human reproductive protein, BOULE, and its prevalence from primitive basal metazoans to chordates. We found that BOULE homologs are present in the genomes of representative species of each of the major lineages of metazoans and exhibit reproductive-specific expression in all species examined, with a preponderance of male-biased expression. Examination of Boule evolution within insect and mammalian lineages revealed little evidence for accelerated evolution, unlike most reproductive genes. Instead, purifying selection was the major force behind Boule evolution. Furthermore, loss of function of mammalian Boule resulted in male-specific infertility and a global arrest of sperm development remarkably similar to the phenotype in an insect boule mutation. This work demonstrates the conservation of a reproductive protein throughout eumetazoa, its predominant testis-biased expression in diverse bilaterian species, and conservation of a male gametogenic requirement in mice. This shows an ancient gametogenesis requirement for Boule among Bilateria and supports a model of a common origin of spermatogenesis. While sexual reproduction is widespread among animals, it remains enigmatic to what extent sexual reproduction is conserved and when sex-specific gametogenesis (spermatogenesis and oogenesis) originated in animals. Here we demonstrate the presence of the reproductive-specific protein Boule throughout bilaterally-symmetric animals (Bilateria) and the conservation of its male reproductive function in mice. Examination of Boule evolution in insect and mammalian lineages, representing the Protostome and Deuterostome clades of bilateral animals, failed to detect any evidence for accelerated evolution. Instead, purifying selection is the major force behind Boule evolution. Further investigation of Boule homologs among Deuterostome species revealed reproduction-specific expression, with a strong prevalence of testis-biased expression. We further determined the function of a deuterostomian Boule homolog by inactivating Boule in mice (a representative mammal, a class of Deuterostomes). Like its counterpart in Drosophila (a representative of the opposing Protostome clade), mouse Boule is also required only for male reproduction. Loss of mouse Boule prevents sperm production, resulting in a global arrest of spermatogenesis in remarkable similarity to that of Drosophila boule mutants. Our findings are consistent with a common origin for male gametogenesis among metazoans and reveal the high conservation of a reproduction-specific protein among bilaterian animals.
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影响因子：
64.8
作者：
Clark, Andrew G.;Eisen, Michael B.;MacCallum, Iain
通讯作者：
MacCallum, Iain
影响因子：
2.7
作者：
Greenbaum, Michael P.;Ma, Lang;Matzuk, Martin M.
通讯作者：
Matzuk, Martin M.
在表现出同步分化的细胞组中，细胞间桥的发生。
DOI：
10.1083/jcb.5.3.453
发表时间：
1959-05-25
期刊：
The Journal of biophysical and biochemical cytology
影响因子：
--
作者：
FAWCETT, D W;ITO, S;SLAUTTERBACK, D
通讯作者：
SLAUTTERBACK, D
影响因子：
64.8
作者：
Chu, Diana S.;Liu, Hongbin;Meyer, Barbara J.
通讯作者：
Meyer, Barbara J.
影响因子：
2.9
作者：
Bachvarova, Rosemary F.;Crother, Brian I.;Johnson, Andrew D.
通讯作者：
Johnson, Andrew D.