A tether for Woronin body inheritance is associated with evolutionary variation in organelle positioning.

A tether for Woronin body inheritance is associated with evolutionary variation in organelle positioning.
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DOI:
10.1371/journal.pgen.1000521
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发表时间:
2009-06
期刊:
影响因子:
4.5
通讯作者:
Jedd G
Jedd G
中科院分区:
生物学2区
文献类型:
--
作者:
Ng SK;Liu F;Lai J;Low W;Jedd G

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真核生物的细胞器进化是为了支持进化相关生物的生活方式。在真菌中,丝状子囊菌具有称为Woronin body (WBs)的密核细胞器。这些细胞器起源于过氧化物酶体,并在细胞损伤时执行封闭间隔孔的适应性功能。在这里,我们确定了一种WB遗传所需的细胞器系链Leashin,并将其与WB分布亚细胞模式的进化变异联系起来。在神经孢子虫中,leashin (lah)位点编码两个相关的相邻基因。LAH-1的n端序列通过WB特异性膜蛋白WSC与WB结合,c端序列通过细胞皮质关联遗传WB。LAH-2定位于菌丝顶端和隔孔边缘,在菌落生长中起作用。在大多数物种中,WBs直接系于孔边缘,然而,神经孢子虫及其近亲已经进化出一种离域的皮层联系模式。利用一种构建染色体编码融合蛋白的新方法,标记融合标记(MFT),我们发现LAH-1/LAH-2融合可以复制神经孢子虫的祖先模式。我们的研究结果确定了WB和细胞皮层之间的联系,并表明leashin的分裂在细胞器定位的适应性进化中发挥了关键作用。在真菌界,被称为菌丝的管状细胞通过尖端延伸和侧分支生长,产生相互连接的多细胞合胞体,这种独特的细胞结构特别适合于觅食、长途运输和侵入性生长。真菌的主要群体已经独立地进化出支持这种多细胞形式的细胞器。Woronin小体在4亿多年前从丝状子囊菌的共同祖先进化而来,并在细胞损伤的反应中执行一种适应性功能,即封闭连接菌丝室的孔(间隔孔)。这项研究确定了Leashin,一种通过提供与细胞皮层的连接来促进Woronin体公平遗传的系缚蛋白。皮层关联模式表现出系统的变异;在大多数丝状子囊菌中,Woronin小体系在间隔孔上。相比之下,最近在以神经孢子虫和索达虫为代表的群体中进化出了一种离域模式。我们提出的证据表明,祖先的leashin基因被分裂成两个独立的转录单位,以允许这种进化转变。这项工作是丝状子囊菌的典范,具有良好的系统发育关系,多样化的测序基因组和强大的单倍体遗传学,为理解功能细胞和生理背景下的进化创新提供了模型系统。
Eukaryotic organelles evolve to support the lifestyle of evolutionarily related organisms. In the fungi, filamentous Ascomycetes possess dense-core organelles called Woronin bodies (WBs). These organelles originate from peroxisomes and perform an adaptive function to seal septal pores in response to cellular wounding. Here, we identify Leashin, an organellar tether required for WB inheritance, and associate it with evolutionary variation in the subcellular pattern of WB distribution. In Neurospora, the leashin (lah) locus encodes two related adjacent genes. N-terminal sequences of LAH-1 bind WBs via the WB–specific membrane protein WSC, and C-terminal sequences are required for WB inheritance by cell cortex association. LAH-2 is localized to the hyphal apex and septal pore rim and plays a role in colonial growth. In most species, WBs are tethered directly to the pore rim, however, Neurospora and relatives have evolved a delocalized pattern of cortex association. Using a new method for the construction of chromosomally encoded fusion proteins, marker fusion tagging (MFT), we show that a LAH-1/LAH-2 fusion can reproduce the ancestral pattern in Neurospora. Our results identify the link between the WB and cell cortex and suggest that splitting of leashin played a key role in the adaptive evolution of organelle localization. In the kingdom Fungi, tubular cells called hyphae grow by tip extension and lateral branching to produce an interconnected multicellular syncytium and this unique cellular architecture is especially suited to foraging, long distance transport, and invasive growth. Major groups of fungi have independently evolved cellular organelles that support this form of multicellularity. Woronin bodies evolved over 400 million years ago in the common ancestor of filamentous Ascomycetes and perform an adaptive function to seal pores that connect hyphal compartments (septal pores) in response to cellular wounding. This study identifies Leashin, a tethering protein that promotes equitable Woronin body inheritance by providing a link to the cell cortex. Patterns of cortex association display systematic variation; in most of the filamentous Ascomycetes, Woronin bodies are tethered to the septal pore. By contrast, a delocalized pattern has recently evolved in a group represented by Neurospora and Sordaria. We present evidence suggesting that the ancestral leashin gene was split into two independent transcription units to permit this evolutionary transition. This work is exemplary of how filamentous Ascomycetes with well-resolved phylogenetic relationships, diverse sequenced genomes and powerful haploid genetics provide model systems for understanding evolutionary innovation within a functional cellular and physiological context.
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