Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects.
Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects.
复制标题
DOI：
10.7554/elife.03676
复制
发表时间：
2014-09-23
期刊：
影响因子：
7.7
通讯作者：
Malik HS
中科院分区：
文献类型：
--
作者：
Drinnenberg IA;deYoung D;Henikoff S;Malik HS
所有真核生物中的染色体分离都依赖于着丝粒，着丝粒是在细胞分裂过程中招募动粒蛋白并介导纺锤体附着的染色体位点。着丝粒组蛋白H3变体CenH 3是大多数真核生物（包括动物、真菌、植物和原生生物）中着丝粒的决定性染色质组分。在这项研究中，使用详细的基因组和转录组分析，我们表明CenH 3在至少四种昆虫谱系中独立丢失。这些谱系中的每一个都代表了从单中心性（着丝粒决定簇定位于单个染色体区域）到全中心性（着丝粒决定簇延伸到整个染色体长度）的独立转变，其历史可以追溯到3亿年前。因此，全着丝粒昆虫含有CenH 3独立的着丝粒，与几乎所有其他真核生物不同。我们建议，古老的过渡到全中心的昆虫避免了需要保持CenH 3，否则是必不可少的，在大多数真核生物，包括其他全中心。DOI：http://dx.doi.org/10.7554/eLife.03676.001细胞分裂是生物体的一个基本重要过程。在真核生物中，如植物和动物，基因组DNA被紧密包装成染色体，需要复制并忠实地分裂成子细胞。染色体的分离是由动粒完成的，动粒是一种蛋白质复合物，它在染色体上组装，并与提供染色体分离力的机器形成连接。着丝粒在称为着丝粒的特殊染色体区域上组装。在大多数真核生物中，动粒组装依赖于一种称为CenH 3的着丝粒蛋白，该蛋白对染色体分离过程至关重要。大多数动物和植物物种是单中心的-染色体的一部分专用于CenH 3加载和着丝粒功能，成对的染色体似乎在单个点或初级缢痕处连接。相比之下，全着丝粒物种的着丝粒活性则沿着配对染色体的全长分布。在进化过程中，全中心性是如何从单中心性产生的仍然不清楚。Drinnenberg等人利用了这样一个事实，即昆虫至少代表了四个独立的从单着丝粒染色体到全着丝粒染色体的转变。有几种昆虫是全着丝粒的，包括蝴蝶和飞蛾、臭虫和虱子、和蜻蜓，而其他昆虫是单着丝粒的，如苍蝇、蜜蜂和甲虫。Drinnenberg等人比较了来自这些昆虫谱系中的每一种的动粒蛋白的所有谱，发现CenH 3在所有检查的全着丝粒昆虫中不存在，但在所有单着丝粒昆虫物种中存在。尽管全着丝粒昆虫失去了CenH 3，但它们仍然有许多动粒蛋白，特别是那些附着在迫使染色体分离的机器上的蛋白。基于进化重建，Drinnenberg等人推断，昆虫中每一次向全着丝粒的独立转变都可能引入着丝粒的变化，从而消除了对其他必需CenH 3蛋白的需求。这项研究挑战了CenH 3在所有真核生物中必不可少的概念。事实上，全着丝粒昆虫，占目前已知真核生物物种生物多样性的16%，似乎已经进化出一种全新的方式来定义它们的着丝粒，与所有其他真核生物不同。DOI：http://dx.doi.org/10.7554/eLife.03676.002网站
Faithful chromosome segregation in all eukaryotes relies on centromeres, the chromosomal sites that recruit kinetochore proteins and mediate spindle attachment during cell division. The centromeric histone H3 variant, CenH3, is the defining chromatin component of centromeres in most eukaryotes, including animals, fungi, plants, and protists. In this study, using detailed genomic and transcriptome analyses, we show that CenH3 was lost independently in at least four lineages of insects. Each of these lineages represents an independent transition from monocentricity (centromeric determinants localized to a single chromosomal region) to holocentricity (centromeric determinants extended over the entire chromosomal length) as ancient as 300 million years ago. Holocentric insects therefore contain a CenH3-independent centromere, different from almost all the other eukaryotes. We propose that ancient transitions to holocentricity in insects obviated the need to maintain CenH3, which is otherwise essential in most eukaryotes, including other holocentrics. DOI: http://dx.doi.org/10.7554/eLife.03676.001 Cell division is a fundamentally important process for living organisms. In eukaryotes, such as plants and animals, genomic DNA is tightly packaged into chromosomes, which needs to be copied and faithfully divided into daughter cells. Segregating the chromosomes is accomplished by the kinetochore, a protein complex that assembles on the chromosome and forms attachments to the machinery that provides the force for chromosome segregation. Kinetochores assemble on specialized chromosomal regions called centromeres. In most eukaryotes, kinetochore assembly relies on a centromeric protein called CenH3 that is essential for the process of chromosome segregation. Most animal and plant species are monocentric—one part of the chromosome is dedicated to CenH3 loading and centromere function and paired chromosomes appear to be joined at a single point, or primary constriction. In contrast, holocentric species instead have centromeric activity distributed along the entire length of the paired chromosomes. How holocentricity arose from monocentricity over the course of evolution remains unclear. Drinnenberg et al. took advantage of the fact that insects represent at least four independent transitions from monocentric to holocentric chromosomes. Several species of insects are holocentric—including butterflies and moths, bugs and lice, earwigs, and dragonflies—while others are monocentric—such as flies, bees, and beetles. Drinnenberg et al. compared the repertoire of kinetochore proteins from each of these insect lineages and found that CenH3 was absent in all the holocentric insects examined but present in all the monocentric insect species. Despite the loss of CenH3 in the holocentric insects, they still had many of the kinetochore proteins—particularly, those proteins that attach to the machinery that forces chromosomes apart. Based on an evolutionary reconstruction, Drinnenberg et al. infer that each independent transition to holocentricity in insects likely introduced changes to the centromere that eliminated the need for the otherwise essential CenH3 protein. This study challenges the notion that CenH3 is essential in all eukaryotes. Indeed, holocentric insects, which make-up 16% of the biodiversity of the currently known eukaryote species, appear to have evolved a completely novel way to define their centromeres, distinct from all the other eukaryotes. DOI: http://dx.doi.org/10.7554/eLife.03676.002