Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
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DOI：
10.1371/journal.pbio.1001197
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发表时间：
2011-11
期刊：
影响因子：
9.8
通讯作者：
Gurdon JB
中科院分区：
文献类型：
--
作者：
Narbonne P;Simpson DE;Gurdon JB
诱导信号和反应的缺陷是两种进化上遥远的蛙种之间核胞质不相容的基础，而特定处理在外植体和整个胚胎中部分恢复了这种反应。在距离足够远的物种中，细胞核和细胞质之间的不相容会导致杂交胚胎和核胞质杂交胚胎发育停滞。已经提出了几种假说来解释它们的致命性，包括胚胎基因组激活（EGA）和/或核-线粒体相互作用的问题。然而，结论性鉴定的原因潜在的发育缺陷的杂交胚胎仍然缺乏。研究表明，尽管非洲爪蟾和热带爪蟾的同种雄激素单倍体均有80%以上发育到游泳蝌蚪期，但由非洲爪蟾卵细胞浆和热带爪蟾精子核结合形成的雄激素单倍体总是不能正常原胚，无法进入游泳蝌蚪期。尽管这种阻滞，这些杂合体在其初始原肠胚缺陷表现的阶段显示出定量正常的EGA和能量水平。这两个物种之间的核细胞质不相容是由多种因素共同导致的，包括来自植物体的诱导信号发射减少，动物细胞对诱导信号的敏感性降低，以及两种物种之间关键胚胎蛋白（Xbra）浓度的差异，这些因素共同导致诱导效率低下和原肠胚形成过程中的收敛延伸缺陷。事实上，增加诱导信号和/或Xbra信号的暴露，部分地恢复了动物外植体和整个杂交胚胎的诱导反应。总之，我们的研究表明，一个物种的卵细胞质可能不支持另一个物种的细胞核促进的发育，即使这个细胞核不干扰卵的细胞质/母体功能，而卵细胞质也能够激活该细胞核的基因组。相反，我们的结果提供了证据，证明物种之间的低效率信号传导和关键蛋白质浓度的差异导致了杂交的发育缺陷。最后，他们表明杂交的不亲和性可以通过适当的处理来纠正。当两个物种分别进化了数百万年，它们各自的基因组积累了许多微小的变化，这些变化共同导致了它们性格上的差异。其中一些会影响卵子在种系内的制备方式和/或胚胎的发育方式，因此特定物种的卵细胞质只能支持其自身基因组或细胞核促进的发育。因此，在遥远物种的进化过程中，细胞质和细胞核之间产生了发育不相容，其机制尚不清楚。我们利用两种进化距离较远的蛙种（非洲爪蟾和热带爪蟾）在一个有利的系统中研究了这一现象。我们发现，在形成形成细胞运动的一个重要过程中，带热带田蚕细胞质和热带田蚕细胞核的杂交蛙胚胎总是存在缺陷。通过一系列的实验，我们解剖和/或重组这些杂交胚胎的一部分，并观察它们在培养中的行为，我们表明，这种现象的发生是因为负责产生这些细胞运动的信号级联出现故障。因此，我们假设低效的分子信号传导导致了这种杂交的死亡。
Defects in induction signaling and response underlie the nucleocytoplasmic incompatibility between two evolutionarily distant frog species, while specific treatments partially restore this response in explants and whole embryos. Incompatibilities between the nucleus and the cytoplasm of sufficiently distant species result in developmental arrest of hybrid and nucleocytoplasmic hybrid (cybrid) embryos. Several hypotheses have been proposed to explain their lethality, including problems in embryonic genome activation (EGA) and/or nucleo-mitochondrial interactions. However, conclusive identification of the causes underlying developmental defects of cybrid embryos is still lacking. We show here that while over 80% of both Xenopus laevis and Xenopus (Silurana) tropicalis same-species androgenetic haploids develop to the swimming tadpole stage, the androgenetic cybrids formed by the combination of X. laevis egg cytoplasm and X. tropicalis sperm nucleus invariably fail to gastrulate properly and never reach the swimming tadpole stage. In spite of this arrest, these cybrids show quantitatively normal EGA and energy levels at the stage where their initial gastrulation defects are manifested. The nucleocytoplasmic incompatibility between these two species instead results from a combination of factors, including a reduced emission of induction signal from the vegetal half, a decreased sensitivity of animal cells to induction signals, and differences in a key embryonic protein (Xbra) concentration between the two species, together leading to inefficient induction and defective convergence-extension during gastrulation. Indeed, increased exposure to induction signals and/or Xbra signalling partially rescues the induction response in animal explants and whole cybrid embryos. Altogether, our study demonstrates that the egg cytoplasm of one species may not support the development promoted by the nucleus of another species, even if this nucleus does not interfere with the cytoplasmic/maternal functions of the egg, while the egg cytoplasm is also capable of activating the genome of that nucleus. Instead, our results provide evidence that inefficient signalling and differences in the concentrations of key proteins between species lead to developmental defects in cybrids. Finally, they show that the incompatibilities of cybrids can be corrected by appropriate treatments. When two species evolve separately for several million years, their respective genomes accumulate many small changes that together are responsible for the differences in their characters. Some of these affect the way eggs are prepared inside the germline, and/or how embryos develop, such that the egg cytoplasm of a given species can only support development promoted by its own genome or nucleus. Thus, developmental incompatibility arises between the cytoplasm and the nucleus of distant species during evolution and we don't know its mechanism. We have studied this phenomenon in an advantageous system using two evolutionarily distant frog species (Xenopus laevis and Xenopus tropicalis). We found that hybrid frog embryos with X. laevis cytoplasm and X. tropicalis nuclei are always defective in an important process that is necessary to generate morphogenetic cell movements during development. Through a series of experiments in which we dissect out and/or recombine parts of such hybrid embryos and observe their behaviour in culture, we show that this phenomenon occurs because of malfunctions in the signalling cascade that is responsible for generating these cell movements. Thus, we postulate that inefficient molecular signalling contributes to the death of such hybrids.
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DOI：
10.1089/clo.2009.0004
发表时间：
2009-06-01
期刊：
CLONING AND STEM CELLS
影响因子：
--
作者：
Chung, Young;Bishop, Colin E.;Lanza, Robert
通讯作者：
Lanza, Robert
影响因子：
1.6
作者：
Fujiwara, A;Abe, S;Yoshida, MC
通讯作者：
Yoshida, MC
影响因子：
2.7
作者：
Conlon, FL;Smith, JC
通讯作者：
Smith, JC
影响因子：
3
作者：
Devenish, RJ;Prescott, M;Nagley, P
通讯作者：
Nagley, P
影响因子：
2.4
作者：
BURKI, E
通讯作者：
BURKI, E