Endosomal transport of septin mRNA and protein indicates local translation on endosomes and is required for correct septin filamentation

Abstract

Endosomes transport lipids and proteins over long distances by shuttling along microtubules. They also carry mRNAs on their surface, but the precise molecular function of this trafficking process is unknown. By live cell imaging of polarized fungal hyphae, we show microtubule-dependent transport of septin mRNA and encoded septin protein on the same shuttling endosomes. Consistent with the hypothesis that septin mRNA is translated on endosomes, the accumulation of septin protein on endosomes requires the recruitment of septin mRNA. Furthermore, ribosomal proteins co-localise with shuttling endosomes, but only if mRNA is present. Importantly, endosomal trafficking is essential for an efficient delivery of septin protein to filaments at growth poles, a process necessary to establish unipolar growth. Thus, we propose that local mRNA translation loads endosomes with septins for assembly and efficient delivery to septin filaments.

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

“…Importantly, both subcellular localizations of Cdc3 depend on Rrm4 (188). Since the presence of both cdc3 mRNA and ribosomes at early endosomes is dependent on Rrm4, the local translation of cdc3 mRNA most likely loads the cytoplasmic surface of endosomes with Cdc3 protein for transport toward the hyphal tip (161,188). Consistently, all four septin mRNAs and proteins localize to early endosomes and are assembled in higher-order filaments.…”

“…Consistently, mRNAassociated ribosomes are transported and distributed identically (172,188). Thus, early endosomes gained a novel function in distributing mRNAs and ribosomes.…”

“…The encoded protein, Cdc3, also accumulates on Rrm4-positive early endosomes and forms higher-order filaments with a gradient emanating from the hyphal tip. Importantly, both subcellular localizations of Cdc3 depend on Rrm4 (188). Since the presence of both cdc3 mRNA and ribosomes at early endosomes is dependent on Rrm4, the local translation of cdc3 mRNA most likely loads the cytoplasmic surface of endosomes with Cdc3 protein for transport toward the hyphal tip (161,188).…”

Kinetic partitioning during de novo septin filament assembly creates a critical G1 “window of opportunity” for mutant septin function

“…18 Here we consider only the temporal component of the putative "window." Despite the fact that budding yeast septin transcription is not obviously coordinated with the cell division cycle, 19 there does appear to be a period of time in the cell cycle during which new septin hetero-oligomers should be assembled.…”

Meeting report – shining light on septins

“…Local translation of septin mRNAs on shuttling endosomes is a new mechanism for orchestrating septin assembly and transport in time and space (Baumann et al, 2014). Michael Feldbrügge (Universität Düsseldorf, Germany) presented work performed in the corn smut Ustilago maydis showing that local translation of all septin mRNAs is needed for the subcellular localization of septins on the surface of endosomes.…”