Close

Altering the temporal regulation of one transcription factor drives sensory trade-offs

Ariane Ramaekers, Simon Weinberger, Annelies Claeys, Martin Kapun, Jiekun Yan, Reinhard Wolf, Thomas Flatt, Erich Buchner, Bassem A. Hassan

Posted on: 19 June 2018

Preprint posted on 15 June 2018

Why do animals with large eyes have small noses and vice versa? By investigating this trade-off mechanism in detail in flies, the Hassan Lab traces it to a single nucleotide polymorphism.

Selected by Mariana R.P. Alves

Background

Across different species, eyes and olfactory organs (such as nose in mammals or antennae in flies) share the same developmental origin. In the fly, their origin is the eye-antennal imaginal disc (EAD). During development, eye and antennal related transcription factors are firstly co-expressed in the EAD, then progressively become restricted in space to form the eye and antennae subdivisions of the EAD before finally mutually repressing each other – a succession of events shared by other organisms. However, a trade-off between vision and olfaction has been observed in different organisms, in the form of phenotypical differences in ratios of eye to olfactory organs. There are cues suggesting that animals make use of this to adapt to the environment, but the mechanisms behind the molecular mechanism of sensory trade-off are still not fully clear. The authors of this preprint explored this question using Drosophila, which exhibits natural variation of eye sizes between and within species.

Key findings

The authors were able to pinpoint the origin of differential proportions of sensory organs both between and within Drosophila species. For this, they focus on eye-size variation, as a marker of vision/olfaction trade-off. They show that this variation originates in development, by differences in the proportion between eye and non-eye multipotent cells in the EAD. This differential proportion is controlled by temporal differences in the regulation of Eyeless (one of the four orthologues of Pax6 in Drosophila): when the segregation into two fields – Eyeless positive and negative – occurs earlier, this leads to increased eye size since Eyeless positive cells proliferate more. The authors traced back this temporally differential regulation between Drosophila species to ortholog enhancers of this gene. When the expression driven by these enhancers retracts from homogenous expression (of eye-antennae factors in the EAD) to the respective subdividing compartment at different velocities, the field segregation occurs at different times.

 

Visual schematic of the model proposed: differential proportion of sensory compartments caused by differential duration of uniform versus heterogeneous growth due to differential posterior retraction of ey. From Ramaekers et al., 2018, Figure 6 (under CC-BY-NC-ND 4.0).

 

This logic is conserved within species. The authors show that the temporal differences observed in two Drosophila melanogaster strains are due to a single nucleotide polymorphism in the enhancer studied: the substitution of a Guanine to an Adenine, which is found in most natural populations of Drosophila melanogaster, with the exception of populations from Sub-Saharan Africa, which are mostly fixed for the Guanine-allele. This SNP is found at a sequence similar to the binding motif of an antennae-related transcription factor (Ct). The authors show causality between impairment of Ct activity (by RNAi knockdown) during EAD development and increased eye size. Experiments with synthetic eyeless enhancers suggest that, when the nucleotide substitution occurs, Ct binds with lower affinity to this enhancer, leading to decreased repression, and ultimately to different timing of EAD-field segregation and increased eye size. The authors finally determined that the eyeless cis regulatory SNP is indeed the cause to eye-size variation by CRISPR/Cas9 genome editing.

In addition, the authors tested the functional readout of facet number into visual acuity between Drosophila strains and saw that increased facet number leads to increased visual acuity, aiding the suggestion of eye-size regulation as an evolutionary mechanism for environment adaptation.

What I like about this preprint

I chose this preprint because I am particularly interested in transcriptional regulation throughout development. I really liked the completeness of this study. The uncovering of mechanisms into the tiniest detail fascinates me, and I feel that this study is very close to that. In addition, since my work is related with transcription factor binding, thus including binding affinities, I am amazed to see yet another study shedding light into the importance and consequences that differential binding affinity might have. In this case, in the “micro-scale”, a SNP causing a site to have lower affinity to a repressor, ultimately has such “macro-scale” phenotypical and functional effect. Finally, I also find it always interesting to learn about behavioural measurements, which I never performed (if you are also curious, check the methods for measurement of visual acuity!).

Open questions

I would be interested to know how important the authors think it would be to confirm if these mechanisms are conserved in vertebrates, and to see if there is a general pattern across animals for the biochemistry and molecular biology behind sensory trade-offs. In addition, in the shorter-term, would it be relevant to look into the regulation of the antennal structures? In this study, the trait measured was always eye-size. Would it possible to distinguish which is the evolutionary target of the adaptation – if vision, olfaction, or both?

 

Tags: drosophila, eyeless, fly, sensory, snp, trade-off

Read preprint (No Ratings Yet)

Have your say

Your email address will not be published. Required fields are marked *

This site uses Akismet to reduce spam. Learn how your comment data is processed.

Sign up to customise the site to your preferences and to receive alerts

Register here

Also in the developmental biology category:

Actin-based deformations of the nucleus control multiciliated ependymal cell differentiation

Marianne Basso, Alexia Mahuzier, Syed Kaabir Ali, et al.

Selected by 30 October 2024

Ryan Harrison

Developmental Biology

HIF1A contributes to the survival of aneuploid and mosaic pre-implantation embryos

Estefania Sanchez-Vasquez, Marianne E. Bronner, Magdalena Zernicka-Goetz

Selected by 11 October 2024

Anchel De Jaime Soguero

Developmental Biology

Axis reset is rate limiting for onset of whole-body regenerative abilities during planarian development

Clare L.T. Booth, Brian C. Stevens, Clover A. Stubbert, et al.

Selected by 10 October 2024

Isabella Cisneros

Developmental Biology

Also in the evolutionary biology category:

Enhancer-driven cell type comparison reveals similarities between the mammalian and bird pallium

Nikolai Hecker , Niklas Kempynck , David Mauduit, et al.

Selected by 02 July 2024

Rodrigo Senovilla-Ganzo

Bioinformatics

Modular control of time and space during vertebrate axis segmentation

Ali Seleit, Ian Brettell, Tomas Fitzgerald, et al.

AND

Natural genetic variation quantitatively regulates heart rate and dimension

Jakob Gierten, Bettina Welz, Tomas Fitzgerald, et al.

Selected by 24 June 2024

Girish Kale, Jennifer Ann Black

Developmental Biology

Fetal brain response to maternal inflammation requires microglia

Bridget Elaine LaMonica Ostrem, Nuria Dominguez Iturza, Jeffrey Stogsdill, et al.

Selected by 24 April 2024

Manuel Lessi

Neuroscience

preLists in the developmental biology category:

BSDB/GenSoc Spring Meeting 2024

A list of preprints highlighted at the British Society for Developmental Biology and Genetics Society joint Spring meeting 2024 at Warwick, UK.

 



List by Joyce Yu, Katherine Brown

GfE/ DSDB meeting 2024

This preList highlights the preprints discussed at the 2024 joint German and Dutch developmental biology societies meeting that took place in March 2024 in Osnabrück, Germany.

 



List by Joyce Yu

‘In preprints’ from Development 2022-2023

A list of the preprints featured in Development's 'In preprints' articles between 2022-2023

 



List by Alex Eve, Katherine Brown

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

The Society for Developmental Biology 82nd Annual Meeting

This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.

 



List by Joyce Yu, Katherine Brown

CSHL 87th Symposium: Stem Cells

Preprints mentioned by speakers at the #CSHLsymp23

 



List by Alex Eve

Journal of Cell Science meeting ‘Imaging Cell Dynamics’

This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.

 



List by Helen Zenner

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

Alumni picks – preLights 5th Birthday

This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.

 



List by Sergio Menchero et al.

CellBio 2022 – An ASCB/EMBO Meeting

This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.

 



List by Nadja Hümpfer et al.

2nd Conference of the Visegrád Group Society for Developmental Biology

Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)

 



List by Nándor Lipták

Fibroblasts

The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!

 



List by Osvaldo Contreras

EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)

A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.

 



List by Alex Eve

EMBL Conference: From functional genomics to systems biology

Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020

 



List by Jesus Victorino

Single Cell Biology 2020

A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.

 



List by Alex Eve

Society for Developmental Biology 79th Annual Meeting

Preprints at SDB 2020

 



List by Irepan Salvador-Martinez, Martin Estermann

FENS 2020

A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020

 



List by Ana Dorrego-Rivas

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

Cell Polarity

Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.

 



List by Yamini Ravichandran

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

3D Gastruloids

A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.

 



List by Paul Gerald L. Sanchez and Stefano Vianello

ASCB EMBO Annual Meeting 2019

A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)

 



List by Madhuja Samaddar et al.

EDBC Alicante 2019

Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.

 



List by Sergio Menchero et al.

EMBL Seeing is Believing – Imaging the Molecular Processes of Life

Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019

 



List by Dey Lab

SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Lung Disease and Regeneration

This preprint list compiles highlights from the field of lung biology.

 



List by Rob Hynds

Young Embryologist Network Conference 2019

Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier

BSCB/BSDB Annual Meeting 2019

Preprints presented at the BSCB/BSDB Annual Meeting 2019

 



List by Dey Lab

Zebrafish immunology

A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.

 



List by Shikha Nayar

Also in the evolutionary biology category:

‘In preprints’ from Development 2022-2023

A list of the preprints featured in Development's 'In preprints' articles between 2022-2023

 



List by Alex Eve, Katherine Brown

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

EMBO | EMBL Symposium: The organism and its environment

This preList contains preprints discussed during the 'EMBO | EMBL Symposium: The organism and its environment', organised at EMBL Heidelberg, Germany (May 2023).

 



List by Girish Kale

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)

A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.

 



List by Alex Eve

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

ECFG15 – Fungal biology

Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome

 



List by Hiral Shah

COVID-19 / SARS-CoV-2 preprints

List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic

 



List by Dey Lab, Zhang-He Goh

1

SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier
Close