Sigmund Sequoia

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We have sent you a verification email. Competing interests The authors declare that no competing interests exist. Author contributions AK, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article. C-HL, Conception and design, Contributed unpublished essential data or reagents.

TH, Conception and design, Analysis and interpretation of data, Drafting or revising the article. The table shows detailed genotypes used in each of the experiments shown in figures and arranged to depict genotypes analysed for each representative image in the figures. In the interests of transparency, eLife includes the editorial decision letter and accompanying author responses. A lightly edited version of the letter sent to the authors after peer review is shown, indicating the most substantive concerns; minor comments are not usually included.

Your article has been favorably evaluated by K VijayRaghavan as Senior editor and three reviewers, one of whom is a member of our Board of Reviewing Editors. The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission. Kulkarni et al. The work builds on and significantly expands on previous work Petrovic and Hummel, The authors show that photoreceptors can use seq levels as a direct molecular representation of their birth order and use this information to achieve layer and column specific targeting.

The strength of the paper lies in the novel and thorough analysis of the role and 'coding' of birth order of neurons in their targeting. This is especially attractive because it formulates a relatively simple developmental algorithm that controls several aspects of neural circuit assembly. In particular, neither the afferent-afferent interaction data nor the seq levels data are as strong as presented, leaving room for different downstream molecular explanation.

Similarly, a simple layer-selection is not sufficient to pre-determine synaptic partners in a crowded, complicated environment. Subsequent patterning processes as well as molecular matchmaking may occur to ultimately specify synapses. Hence, while the core data on seq-dependent pre-patterning in layer formation remain a strong and important contribution, the authors should clarify and focus the paper on its core for a strong contribution to eLife and the field.

It is most clearly demonstrated in a series of experiments published in two papers, Timofeev et al. Here the L3 growth cone in the M3 layer is essential for the targeting of R8. This is, at least, in part mediated by Netrin signaling; Netrin is expressed selectively in M3 and its receptor Frazzled is expressed and required in R8. This is one possible explanation of an interesting set of data but by no means the only one. This alone, however, does not provide strong support for a direct interaction; the medulla neuropile even at this early stage of development contains the processes of many different neuronal cell types.

Thus, the interactions leading to appropriate segregation may be very indirect.

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The experiments presented in the paper are well done and interesting. But the interpretations are simply not straightforward given the complexity of the experimental design on one hand and the inherent complexity of the tissue. The authors argue that these interactions are sufficient to determine synaptic specificity.

That is, layer-specificity determines synaptic specificity. With the connectome in hand from the Janelia group there are many examples that this is simply not the case. Each layer contains the processes of many different neurons and yet R7 and R8 within their respective layers only make synaptic connections with a discrete subset of them. There is simply no correlation between the area of contact and the probability of synaptic connectivity.

The authors provide one example by showing that R8s misexpressing Seq, within a particular time frame during development, will mistarget to M6 and here, using a clever variation on GRASP they demonstrate synapses between R8 and Dm8, the normal target for R7. Based on this observation, and solely on this observation, they conclude that synaptic specificity is determined by the layer in which a terminal finds itself rather than through selective recognition between processes of different neurons within the same layer. The assumption here, of course, is that expression of Seq has no effect on R8 terminals other than re-positioning it to M6; that is the authors assume that an otherwise normal R8, that is mispositioned, is forming synapses with a target appropriate for this layer.

It is simply not plausible that over expression of a transcription factor that is leading to a change in the position of the growth cone is also not changing its molecular nature. So while the results with sequoia mis-expression are consistent with the notion that layers are determinative for specificity, the data are merely a correlation and one resting on the assumption that mis-expression of Seq during a specific time period has not activated the expression of proteins in these mutant R8 cells for competence to form synapses with Dm8. Later in the manuscript, the authors propose that R7 axons get stuck in M1 in flies that are both seq mutant and gogo overexpressing is their attachment to R8s.

However, gogo is overexpressed with the GMR promoter in these experiments. This means gogo may affect R7s independently from R8s, resulting in their failure to extend to the M3 later. The authors further state that Discussion, second paragraph seq mutant R7 axons extend to M3 later because of their association with R8 axons also reference need for statement that R7 cells are Frazzled-negative.

However, CadN mutant R7 axons that have previously retracted are capable of re-extension in the medulla seemingly independent of what R8s are doing and clearly at the wrong time days later! Ozel et al. A simple experiment here would be to overexpress gogo specifically in seq mutant R8s and observe the behavior of seq mutant R7 cells. The authors use the term 'temporal layer' equally for R7 and R8.

However, R8 indeed actively extends from an initially targeted temporary layer, whereas R7 remains stabilized seemingly in stable interaction with Dm8 throughout medulla expansion Ting et al.

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The wording 'temporal layer' does not apply to R7, since it remains stabilized throughout development and doesn't move anywhere. The authors should come up with a different term for the 'temporary' state of R7 and R8 in this system. One interpretation of the data is that R7 axons as well as Seq overexpressing R8 axons target directly to the future M6 layer, which significantly simplifies the developmental problem at hand.

The apparent movement or 'elongation' happens only because the entire M6 layer is pushed further down by the newly innervating lamina and medulla cells forming the other layers. The authors should replace that with "R7 target layer", "the future M6" or even simply M6. The aims, methods and conclusions might be made a bit clearer. The model based on "relative levels" here is not obvious.

Relativity implies that these axons have a way of communicating their Seq expression level to each other, but I am not sure there is evidence for this? If Seq levels are decreased or increased equally in all cells involved, there should be no defects as the "relative" levels do not change.

To support the hypothesis of 'relative level comparison' one might present an experiment where Seq expression level changes in a subset of cells cause a defect but the same amount of change in all cells does not. If such an experiment is not feasible, the arguments and discussions dealing with comparisons of relative levels should be re-evaluated.

It is surprising that the authors observed Seq expression reduced the early-stage R7 retractions in CadN mutants since they had previously proposed sequoia action through modification of CadN levels Petrovic and Hummel, However, the ratio of retracted R7 axons at P24 is actually quite low very likely to see a normal R7 cell no matter what. The weakness, however, lies in the author's statement that the pre-patterning they describe controls 'synaptic partner matching'.

The developmental step of growth cone segregation between R7 and R8 we describe in the manuscript can be controlled by axon-target interaction, axon-axon interaction or both. Although there is no experimental demonstration of direct R7-R8 afferent interactions, the following set of data indicate that such interactions occur during development.

In addition, in the manuscript we show that the final target layer of sequoia mutant R7 axons depends on the targeting of R8 axons, suggesting that mis-targeting of sequoia mutant R7 axons to ectopic synaptic layer is the consequence of segregation defects rather than a change in target layer recognition.

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This would be the case for a non-cell autonomous function, e. In a scenario in which Seq is critical in the responding cell, e. As we could demonstrate a cell-autonomous function of Seq in R8 for columnar segregation as well as in R7 for layer segregation we envision a mechanistic model related to the concept of cell competition, in which strong cell-cell interactions resulting in cell-autonomous responses discussed in the manuscript.

The types of neurons present in the medulla at the time of R8 and R7 axon innervation remains unknown. Based on data from Li et al. We expect that some form of temporal coordination of afferent axons and their post-synaptic partner cell neurites would actually simplify the synaptic partner matching.

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  4. We fully agree with the criticism and thank the reviewers for raising this issue. We did not intend to state that initial layer identity specifies synaptic partner matching in subsequent steps of development. The cellular complexity of potential postsynaptic target cells for R cell axons has not been fully determined, leaving room for selective mechanisms for synaptogenesis within a layer.

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