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

Ng SK, Liu F, Lai J, Low W, Jedd G - PLoS Genet. (2009)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Temasek Life Sciences Laboratory and Department of Biological Sciences, National University of Singapore, Singapore.

ABSTRACT
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.

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Model for the evolution of Woronin body tethering in the Pezizomycotina.(A) Legend indicates symbols used to depict domains of the Leashin tether. (B) The minimal events associated with splitting of the ancestral leashin locus are indicated. (C) Model for septal pore associated WB-tethering in most of the Pezizomycotina. (D) Model of WB tethering in Neurospora and Sordaria. The double-headed arrow indicates extensive protoplasmic streaming that can be observed in Neurospora and Sordaria (See Video S1).
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pgen-1000521-g007: Model for the evolution of Woronin body tethering in the Pezizomycotina.(A) Legend indicates symbols used to depict domains of the Leashin tether. (B) The minimal events associated with splitting of the ancestral leashin locus are indicated. (C) Model for septal pore associated WB-tethering in most of the Pezizomycotina. (D) Model of WB tethering in Neurospora and Sordaria. The double-headed arrow indicates extensive protoplasmic streaming that can be observed in Neurospora and Sordaria (See Video S1).

Mentions: Our analysis suggests that three events were required to evolve lah-1 and lah-2 from a single ancestral locus (Figure 7). These are - evolution of promoter sequences for independent production of lah-2, intragenic termination for the production of lah-1 and acquisition of a new cortex-binding domain in lah-1. Splicing at intron 10 results in an alternative exon that terminates with a stop codon immediately upstream of the lah-2 promoter region (Figure 5A). MFT tags in this exon are enriched between the WB and cell cortex (Figure 5C) and this region is required for WB inheritance (Figure 2), suggesting that C-terminal sequences of LAH-1 constitute a new cortex-binding domain.


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

Ng SK, Liu F, Lai J, Low W, Jedd G - PLoS Genet. (2009)

Model for the evolution of Woronin body tethering in the Pezizomycotina.(A) Legend indicates symbols used to depict domains of the Leashin tether. (B) The minimal events associated with splitting of the ancestral leashin locus are indicated. (C) Model for septal pore associated WB-tethering in most of the Pezizomycotina. (D) Model of WB tethering in Neurospora and Sordaria. The double-headed arrow indicates extensive protoplasmic streaming that can be observed in Neurospora and Sordaria (See Video S1).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2690989&req=5

pgen-1000521-g007: Model for the evolution of Woronin body tethering in the Pezizomycotina.(A) Legend indicates symbols used to depict domains of the Leashin tether. (B) The minimal events associated with splitting of the ancestral leashin locus are indicated. (C) Model for septal pore associated WB-tethering in most of the Pezizomycotina. (D) Model of WB tethering in Neurospora and Sordaria. The double-headed arrow indicates extensive protoplasmic streaming that can be observed in Neurospora and Sordaria (See Video S1).
Mentions: Our analysis suggests that three events were required to evolve lah-1 and lah-2 from a single ancestral locus (Figure 7). These are - evolution of promoter sequences for independent production of lah-2, intragenic termination for the production of lah-1 and acquisition of a new cortex-binding domain in lah-1. Splicing at intron 10 results in an alternative exon that terminates with a stop codon immediately upstream of the lah-2 promoter region (Figure 5A). MFT tags in this exon are enriched between the WB and cell cortex (Figure 5C) and this region is required for WB inheritance (Figure 2), suggesting that C-terminal sequences of LAH-1 constitute a new cortex-binding domain.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Temasek Life Sciences Laboratory and Department of Biological Sciences, National University of Singapore, Singapore.

ABSTRACT
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.

Show MeSH