A Tether for Woronin Body Inheritance Is Associated with Evolutionary Variation in Organelle Positioning

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.

The HEX1 Gene of Fusarium graminearum Is Required for Fungal Asexual Reproduction and Pathogenesis and for Efficient Viral RNA Accumulation of Fusarium graminearum Virus 1

“…After WB biogenesis in the peroxisome membrane, the newly formed WB should be moved near a septal pore if it is to contribute to septal-pore sealing. In this relocation of the organelle, the Leashin (Lah) gene product is responsible for WB tethering (22). It is also well known that some plant viruses use peroxisomes for their viral replication (43).…”

“…Especially in the case of Tomato bushy stunt virus (TBSV), viral RNA replication occurs on the surface of the cytosolic membrane of peroxisomes in plants and in yeast (44). Based on the previous reports concerning WB biogenesis (21,22,42) and RNA viral replication on peroxisomes and on the current results concerning the presence of gene homologs related to WB biogenesis in F. graminearum (WSC for locus FGSG_01049 and Lah for locus FGSG_04119), it is tempting to speculate that FgV1 or other potential mycoviruses might use this tethering process to facilitate the accumulation and intracellular movement of viral RNAs.…”

“…The Hex1 protein self-assembles to form the Woronin body (WB). The WB is a peroxisome-derived dense-core microbody that is specific to filamentous ascomycetes (21)(22)(23)(24)(25)(26)(27)(28)46). WBs maintain cellular integrity by sealing the septal pore after cellular damage in Neurospora crassa (23)(24)(25).…”

A Large Nonconserved Region of the Tethering Protein Leashin Is Involved in Regulating the Position, Movement, and Function of Woronin Bodies in Aspergillus oryzae

“…Although filamentous fungi are classified as multicellular organisms, septa do not completely separate adjacent hyphal cells due to the presence of a septal pore, which allows the passage of cytoplasm and organelles between adjacent cells (1)(2)(3). Cytoplasmic continuity through the septal pore is associated with the catastrophic risk of cytoplasmic loss in the event of hyphal wounding.…”

Mushrooms: Morphological complexity in the fungi

“…If size does not matter, and the developmental complexity and tissue differentiation seen in these microscopic fungi reflect that seen in mushrooms and truffles, comparison of genetically tractable species with C. cinerea and relatives should also pay dividends. A pair of membranous organelles worth investigating might be the Woronin body of Ascomycota and the septal pore complex of Basidiomycota, which function to seal damaged hyphae and might have been instrumental in allowing fungi to make complex, multicellular structures (19). Making the comparisons suggested herein, most of which can be attempted with existing genome assemblies, might not only unravel the basis of fungal complexity, but point the way for studies of plants and animals, as more of the much larger genomes found in those kingdoms become available.…”