Species-specific developmental timing dictates expansion of the avian wing skeletal pattern

In this preprint, Holly Stainton and Matthew Towers investigate the differences in developmental pace in proximo-distal wing patterning across birds. In the developing wing of quail and chick, the downregulation of Fgf8 expression, Sox9 onset of expression, and necrotic changes occur at equivalent Hamburger-Hamilton (HH) stages, which correspond to 46 chronological stages in bird development. Similarly, Hoxa11 and Hoxa13 follow equivalent dynamics in both species. However, there is a sustained 12-hour difference in the dynamics of expression of these genes between quail and chick that indicates that quail proximo-distal wing patterning progresses faster in comparison to chick. Strikingly, the growth rates are comparable between the species during the patterning phase.

 

In this preprint, the authors perform a series of homochronic transplants to investigate what sets the tempo. As the offset in timing is initiated 12 hours after the HH18/19 stage, the authors perform interspecies polarising region grafts prior to any offset in developmental timing. Whereas Shh expression is downregulated after 48 hours in normal quail wing development, Shh expression in quail grafts placed on chick hosts is extended for 48 hours, matching Shh chick expression at HH26. Likewise, when they perform the reverse transplants grafting chick cells on quail, they are able to show an accelerated decrease in SHH expression of the chick graft transplanted in the quail host at 48 hours later. These experiments indicate that the pace of expression is set at the onset of proximo-distal patterning in wing buds, at the time that the chick and quail HH stage is equivalent.

The authors then looked into retinoic acid (RA) signaling, as it is cleared in the distal region of the wing bud by HH21, and could cause the different behaviour between the HH18/19 stage and the subsequent time points. They found that Cyp26b1 levels rise significantly faster in the quail compared to the chick. As Cyb26b1 is the major retinoic acid degrading enzyme, these findings indicate a decreased degradation rate of retinoic acid in the wing bud of larger species. Moreover, by transiently prolonging retinoic acid signalling, the authors elegantly demonstrate that Shh expression timing is delayed in the quail polarising region graft, as the expression is maintained for approximately the same duration as in the host chick polarising region.

 

To conclude the paper, the authors characterize the dynamics of wing development in turkey. Turkey wings are larger in size than chick, and the preprint shows that they progress with a 12-hour delay in the expression of Shh, Hoxa11 and Hoxa13 compared to chick. As predicted from their findings of the involvement of RA in setting the pace, culturing chick wings with RA from HH18/19 delayed the pace of chick development and matched the length of the chicken wing to that of the turkey at HH21. Altogether, the preprint shows that there is a proportional patterning and temporal scaling in wing bud development between quail, chick, and turkey that can be reset by addition of retinoic acid within the first 12 hours of wing development.

Why I chose the paper and how it moves the field forward:

I’m interested in understanding how developmental timing operates at the cellular level, and this work studies developmental timing in vivo during proximo-distal limb development in birds. Limbs are one of the best characterized developmental systems, and they show a well-defined sequence of temporal events that can be used to investigate developmental tempo. In addition, limbs have undergone extensive evolutionary diversification across species. Moreover, birds are a great model in developmental biology as eggs can easily be collected and cultured, and are amenable for numerous embryology perturbations. Even though chick is the dominant model, reports in quail, zebra finch and emus have provided some interesting developmental evolutionary perspectives (Uygur et al., 2016; Young et al., 2019). I find particularly useful for the of study developmental pace the fact that HH staging is based on morphological features that correspond quite neatly with changes in gene expression programs.

Notably, Stainton and Towers show that developmental timing is proportionately scaled across turkey, chick and quail and demonstrate that RA can delay the timing of wing bud development in quail and chick, suggesting that the degradation rate of RA sets the tempo in the system. This finding resembles the differences in protein degradation observed in mouse and human cells that associate with differences in developmental tempo (Matsuda et al., 2020; Rayon et al., 2020). It would be really exciting to know how Cyp26b1 levels are regulated to modify the degradation rate of RA in their system. Looking forward to their future work!

 

 

Posted on: 4 May 2021

doi: https://doi.org/10.1242/prelights.28815

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