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mRNA transport in fungal top models

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Eukaryotic cells rely on the precise determination of when and where proteins are synthesized. Spatiotemporal expression is supported by localization of mRNAs to specific subcellular sites and their subsequent local translation. This holds true for somatic cells as well as for oocytes and embryos. Most commonly, mRNA localization is achieved by active transport of the molecules along the actin or microtubule cytoskeleton. Key factors are molecular motors, adaptors, and RNA‐binding proteins that recognize defined sequences or structures in cargo mRNAs. A deep understanding of this process has been gained from research on fungal model systems such as Saccharomyces cerevisiae and Ustilago maydis. Recent highlights of these studies are the following: (1) synergistic binding of two RNA‐binding proteins is needed for high affinity recognition; (2) RNA sequences undergo profound structural rearrangements upon recognition; (3) mRNA transport is tightly linked to membrane trafficking; (4) mRNAs and ribosomes are transported on the cytoplasmic surface of endosomes; and (5) heteromeric protein complexes are, most likely, assembled co‐translationally during endosomal transport. Thus, the study of simple fungal model organisms provides valuable insights into fundamental mechanisms of mRNA transport boosting the understanding of similar events in higher eukaryotes. WIREs RNA 2018, 9:e1453. doi: 10.1002/wrna.1453 This article is categorized under: RNA Interactions with Proteins and Other Molecules > Protein–RNA Recognition RNA Interactions with Proteins and Other Molecules > RNA–Protein Complexes RNA Export and Localization > RNA Localization
Microtubule‐dependent mRNA transport in Ustilago maydis. (a) Micrograph (top) and model (bottom) of hypha that expands from an initial yeast‐like cell by polarized growth at the apical pole. Septa are inserted in regular intervals resulting in empty sections at the basal pole. Note that the lab strain used (AB33) was genetically modified so that hyphal growth can be elicited efficiently and independent from mating. In contrast to dikaryotic wild‐type hyphae, the lab strain contains only a single nucleus positioned in the cell center. Organelles such as ribosomes, peroxisomes, as well as mRNPs are transported by early endosomes along antiparallel microtubule arrays. Scale bar: 10 μm. (b) Schematic model of the transport complex of endosomes with an mRNP. Early endosomes are transported by Kin3 and Dynein. According to the results obtained in Aspergillus nidulans, the small GTPase Rab5a is proposed to directly bind to components of the FHF complex that interact with the dynein supercomplex. The RBPs Rrm4 and Pab1 bind directly to endosomal protein Upa1. This interaction is mediated by the MLLE domains of Rrm4 and Pab1. Further components associated with this transport complex are peroxisomes and ribosomes. The presence of the latter suggests active translation of transported mRNAs. (c) Coordinated transport and translation of septin mRNA on shuttling endosomes promotes the assembly of heteromeric septin complexes, and subsequently, the formation of higher order structures like septin filaments at the hyphal tip.
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Actin‐dependent mRNA transport in Saccharomyces cerevisiae. (a) In a budding cell ASH1 mRNA is transported along actin tracks to the daughter cell for translation. Ash1p ends up in the daughter cell, where it is imported into the nucleus (n) for specific inhibition of HO expression. (b) Assembly of the transport mRNP is initiated in the nucleus. ASH1 mRNA is bound co‐transcriptionally by She2p as well as Loc1p and Puf6p. This complex has modest specificity (open lock). Upon transition of the nucleolus (no), export and binding by She3p the mRNP is remodeled and locked in its transport competent form. (c) During transport, the ASH1 mRNA is translationally silenced by the action of the RBPs Khd1p, Puf6p, and Dhh1p. At its destination in the daughter cell Khd1p and Puf6p are released by phosphorylation. This results in the local translation of Ash1p, which is subsequently imported in the daughter nucleus (n). (d) Alternative actin‐dependent transport mechanism involves the ER. Two RBPs associate transported mRNA cargo with the ER. Scp160 binds its mRNA cargo, which is translated at, and thereby tethered to, the ER. In contrast, She2p is able to bind specifically to the ER tubules by recognizing their membrane curvature, as well as by potentially interacting with an ER‐associated orphan adaptor protein.
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RNA Export and Localization > RNA Localization
RNA Interactions with Proteins and Other Molecules > RNA–Protein Complexes
RNA Interactions with Proteins and Other Molecules > Protein–RNA Recognition

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