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
中科院分区:
文献类型:
--
作者:
Ng SK;Liu F;Lai J;Low W;Jedd G
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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影响因子:
3
作者:
Jin, Yuan;Allan, Sabrina;Versaw, Wayne K.
通讯作者:
Versaw, Wayne K.
影响因子:
7.5
作者:
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影响因子:
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作者:
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通讯作者:
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DOI:
10.1099/00221287-144-7-1721
发表时间:
1998-07-01
期刊:
MICROBIOLOGY-UK
影响因子:
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作者:
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通讯作者:
Boekhout, T
影响因子:
11.8
作者:
Cerveny, Kara L.;Studer, Seth L.;Sesaki, Hiromi
通讯作者:
Sesaki, Hiromi