Comparative Hox genes expression within the dimorphic annelid Streblospio benedicti reveals patterning variation during development
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Abstract
Hox genes are transcriptional regulators that elicit cell positional identity along the anterior-posterior region of the body plan across different lineages of Metazoan. Comparison of Hox gene expression across distinct species reveals their evolutionary conservation, however their gains and losses in different lineages can correlate with body plan modifications and morphological novelty. We compare the expression of eleven Hox genes found within Streblospio benedicti, a marine annelid that produces two types of offspring with distinct developmental and morphological features. For these two distinct larval types, we compare Hox gene expression through ontogeny using HCR (hybridization chain reaction) probes for in-situ hybridization and RNA-seq data. We find that Hox gene expression patterning for both types is typically similar at equivalent developmental stages. However, some Hox genes have spatial or temporal differences between the larval types that are associated with morphological and life-history differences. This is the first comparison of developmental divergence in Hox genes expression within a single species and these changes reveal how body plan differences may arise in larval evolution.
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In this manuscript, the authors characterize the expression of Hox genes in two morphs of the marine annelid Streblospio benedicti through in situ hybridization chain reaction (HCR) and time-course RNA-Seq analysis.
Despite some important morphological and life history differences between the two morphs, the authors observe broad similarity of Hox gene expression, with the exception of a few Hox genes that are expressed in swimming setae, which are found in one morph but not another.
Due to differences in the developmental rate of these two morphs, as well as physiological differences, such as embryo size, the authors find it difficult to definitively determine the source of differences between the two life histories. The authors conclude that Hox expression is not the primary driver of life history differences between these morphs. The …
In this manuscript, the authors characterize the expression of Hox genes in two morphs of the marine annelid Streblospio benedicti through in situ hybridization chain reaction (HCR) and time-course RNA-Seq analysis.
Despite some important morphological and life history differences between the two morphs, the authors observe broad similarity of Hox gene expression, with the exception of a few Hox genes that are expressed in swimming setae, which are found in one morph but not another.
Due to differences in the developmental rate of these two morphs, as well as physiological differences, such as embryo size, the authors find it difficult to definitively determine the source of differences between the two life histories. The authors conclude that Hox expression is not the primary driver of life history differences between these morphs. The authors note some heterochronies in Hox expression, but acknowledge that some of these may be a result of differences in staging between the two morphs.
It would be interesting to see if the authors could perform a genetic or chemical manipulation of each morph to cause it to alter its life history. Such a perturbation might make it easier to compare developmental trajectories within a shared physiological background, without the confounding properties of the two morphs examined in this study, which also came from geographically distinct populations.
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Heterochronies across species are difficult to detect due to the methodological barriers of assigning equivalent stages across divergent species.
Are there other kinds of genetic circuits, aside from the segmentation/regionalization hierarchy that you could examine which could be more easily analogized across the two morphs to create a "clock" which could be compared across the morphs? Perhaps eye development and looking at the cell types and morphology of the eyes?
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Lecithotrophic worms were collected from Long Beach (California) and planktotrophic worms from Newark Bay (New Jersey; Zakas et al., 2018).
How similar or different are the genomes of these two morphs? Are there any polymorphisms that distinguish the populations and could be relevant to differences in their development? Are there manipulations that can be performed to change the developmental trajectory of one population into the other, or vice versa? (I'm unfortunately not able to access the Zakas review, these may be obviously answered there).
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downstream of
upstream of?
For example, the swimming setae appear to emerge prior to the expression of Pb, suggesting that processes other than Hox, which precede (upstream of) Hox expression, drive the development of this structure, which then later expresses regional identity markers such as Pb.
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HCR in situ hybridization
Were DAPI stains also performed on these samples? If they were, providing those might make it somewhat easier to interpret precise segment boundaries and relative expression patterns across the samples.
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Yellow dashed lines encircle confirmed autofluorescent regions.
The autofluorescent regions in the samples for the lecithotrophic and plantotrophic regions differ at the same developmental stage (e.g. 2-eye, Hox1/Lab). Is this a result specifically of variability in sample preparation, or a consequence of differences in embryo / cell size, and therefore different quantities of yolk autofluorescence?
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Yellow dashed lines encircle confirmed autofluorescent regions.
Based on the methods detailed below, my understanding is that some of these hybridizations were imaged using different fluorescent channels. To aid understanding of autofluorescence, it might be helpful to false-color these images based on the fluorescent channel used for the hairpin (e.g. green for 488, red for 546, etc.) This could make it more obvious that the setae in the Post2 early plantotrophic stage are visible due to autofluorescence rather than genuine staining. You might also consider adding that detail directly to the figure legend, as the other reference to this artifact is only found in the methods.
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This indicates that there are no duplication events for the Hox genes in the genome and gives high confidence that the Hox gene assignments are correct.
Were there any plausible splice isoforms of the Hox genes identified in your RNA-Seq data?
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We blasted known Hox genes from other spiralian species against our transcriptome to identify homologs in S. benedicti.
Was the BLAST also performed reciprocally? Could you perhaps use a phylogenomic tool for ortholog detection, such as OrthoFinder, to systematically group genes across species into orthogroups?
We've also developed a phylogenomic workflow called NovelTree that builds on top of OrthoFinder to perform a variety of phylogenomic analyses, which might help systematically identify conserved genes across the spiralian species you work on.
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