Drosophila mRNA Localization During Later Development: Past, Present, and Future

Abstract

Multiple mechanisms tightly regulate mRNAs during their transcription, translation, and degradation. Of these, the physical localization of mRNAs to specific cytoplasmic regions is relatively easy to detect; however, linking localization to functional regulatory roles has been more difficult to establish. Historically, Drosophila melanogaster is a highly effective model to identify localized mRNAs and has helped identify roles for this process by regulating various cell activities. The majority of the well-characterized functional roles for localizing mRNAs to sub-regions of the cytoplasm have come from the Drosophila oocyte and early syncytial embryo. At present, relatively few functional roles have been established for mRNA localization within the relatively smaller, differentiated somatic cell lineages characteristic of later development, beginning with the cellular blastoderm, and the multiple cell lineages that make up the gastrulating embryo, larva, and adult. This review is divided into three parts—the first outlines past evidence for cytoplasmic mRNA localization affecting aspects of cellular activity post-blastoderm development in Drosophila. The majority of these known examples come from highly polarized cell lineages such as differentiating neurons. The second part considers the present state of affairs where we now know that many, if not most mRNAs are localized to discrete cytoplasmic regions in one or more somatic cell lineages of cellularized embryos, larvae or adults. Assuming that the phenomenon of cytoplasmic mRNA localization represents an underlying functional activity, and correlation with the encoded proteins suggests that mRNA localization is involved in far more than neuronal differentiation. Thus, it seems highly likely that past-identified examples represent only a small fraction of localization-based mRNA regulation in somatic cells. The last part highlights recent technological advances that now provide an opportunity for probing the role of mRNA localization in Drosophila, moving beyond cataloging the diversity of localized mRNAs to a similar understanding of how localization affects mRNA activity.

Photosystem Biogenesis Is Localized to the Translation Zone in the Chloroplast of Chlamydomonas

“…The T-zone is among a growing number of examples of localized translation for biogenesis and pattern formation in diverse organisms. In the cytoplasm of yeast, neurons, and developing embryos, the translation of specific mRNAs is localized to RNA granules, membrane-bound organelles, or synapses for diverse functions (Lui et al, 2014;Hughes and Simmonds, 2019;Panasenko et al, 2019). An analogous region to the T-zone of the chloroplast was recently reported in mitochondria, the other semiautonomous organelle, for the biogenesis of the respiratory electron transport chain complexes (Stoldt et al, 2018).…”

A putative stem-loop structure in Drosophila crumbs is required for mRNA localisation in epithelia and germline cells

“…In-situ hybridisations essentially followed previous protocols (Jambor et al, 2015;Tomancak et al, 2002). Post-fixed embryos and ovaries were incubated in pre-hybridisation buffer (50% Formamide, 20% of 20x SSC (NaCl 3M, NaCit 300mM), 0.01% Tween-20, volume made up with DEPC treated water) for one hour at 57°C.…”

Pinpointing Cell Identity in Time and Space

“…This, in turn, can influence the cell’s function and capacity to respond to various environmental cues. Additionally, we may observe spatial positioning of certain transcripts in close association with subcellular landmarks or organelles ( Savulescu et al, 2019 , reviewed in Suter, 2018 ; Hughes and Simmonds, 2019 and others) ( Figure 1D ), including membraneless organelles such as stress granules (for example Khong et al, 2017 ; Padrón et al, 2019 ; Wilbertz et al, 2019 ). This could indicate a functional relationship between the RNA’s cellular role and broader cellular processes, such as cell division, differentiation, polarization etc.’ Further, this may also influence, or be influenced by, cell state or identity.…”