Biology subjects

Devan, S. K.

Publications and source records attributed to Devan, S. K..

2 recordsLinked to original sources

bioRxiv2026

Endosomal mRNA transport coordinates local mitochondrial bioenergetics during polar fungal growth

Mitochondrial function relies on the precise spatial coordination of protein synthesis and import. Most mitochondrial proteins are nuclear-encoded and must be supplied across varying intracellular distances. In highly polarized cells such as fungal hyphae and neurons, active long-distance mRNA transport is thought to sustain distal mitochondrial function, but its mechanistic coupling to protein import and organelle physiology is unclear. Here, we demonstrate that endosomal transport of mRNAs encoding mitochondrial proteins orchestrates local bioenergetics in infectious hyphae of Ustilago maydis. Using the subunit Atp3 of electron transport chain Complex V as a model, we uncover that the endosomal mRNA transporter Rrm4 is required for efficient mitochondrial protein import, particularly at growth poles. Loss of Rrm4 leads to defects in mitochondrial import, resulting in altered physiology. We propose that endosome-coupled mRNA transport constitutes a fundamental layer of subcellular mitochondrial homeostasis, with implications extending from fungal pathogenicity to neuronal disease. Significance StatementFungal pathogens depend on efficient polar growth to execute their infection programs. Consequently, their growing cell poles face a massive local demand of energy, which is supplied by mitochondria. Currently, it is unclear how involved proteins of the mitochondrial electron transport chain (ETC) reach these distant organelles. Here, we combine fungal genetics, metabolomics, transcriptomics and minimal invasive live-cell imaging to resolve this spatial challenge in the corn pathogen Ustilago maydis. We discover that long-distance endosomal hitchhiking of mRNAs encoding mitochondrial ETC components is essential to sustain active mitochondria at the expanding pole. Ultimately, this membrane-coupled mRNA trafficking precisely orchestrates subcellular mitochondrial function, disclosing a previously unrecognized Achilles heel for the development of novel fungicides.

microbiology↗

bioRxiv2024

Deciphering the RNA-binding protein network during endosomal mRNA transport

Microtubule-dependent endosomal transport is crucial for polar growth, ensuring the precise distribution of cellular cargos such as proteins and mRNAs. However, the molecular mechanism linking mRNAs to the endosomal surface remains poorly understood. Here, we present a structural analysis of the key RNA-binding protein Rrm4 from Ustilago maydis. Our findings reveal a new type of MademoiseLLE domain featuring a seven-helical bundle that provides a distinct binding interface. A comparative analysis with the canonical MLLE domain of the poly(A)-binding protein Pab1 disclosed unique characteristics of both domains. Deciphering the MLLE binding code enabled prediction and verification of previously unknown Rrm4 interactors containing short linear motifs. Importantly, we demonstrated that the human MLLE domains, such as those of PABPC1 and UBR5, employed a similar principle to distinguish among interaction partners. Thus, our study provides unprecedented mechanistic insights into how structural variations in the widely distributed MLLE domain facilitates mRNA attachment during endosomal transport. SignificancePolar growing cells, such as fungal hyphae and neurons, utilize endosomes to transport mRNAs along their microtubules. But how do these mRNAs precisely attach to endosomes? Our study addresses this question by investing the key mRNA transporter, Rrm4, in a fungal model microorganism. We uncovered new features of a protein-protein interaction domain that recognizes specific short linear motifs in binding partners. While this domain resembles one found in the poly(A)-binding protein, it exhibits distinct motif recognition. Deciphering the underlying binding code unveiled new interaction partners for Rrm4. The recognition system is used to form a resilient network of RNA-binding proteins (RBPs) and their interaction partners during endosomal transport. This principle is applicable to humans, highlighting its fundamental importance.

microbiology↗