rst transcriptional activity influences kirre mRNA concentration in the Drosophila pupal retina during the final steps of ommatidial patterning.

<h4>Background</h4>Drosophila retinal architecture is laid down between 24-48 hours after puparium formation, when some of the still uncommitted interommatidial cells (IOCs) are recruited to become secondary and tertiary pigment cells while the remaining ones undergo apoptosis. This choi...

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Main Authors: Maiaro Cabral Rosa Machado, Shirlei Octacilio-Silva, Mara Silvia A Costa, Ricardo Guelerman P Ramos
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21857931/?tool=EBI
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spelling doaj-8f144b4e376e4900ba6aa6b82f3b22922021-03-04T01:40:40ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-0168e2253610.1371/journal.pone.0022536rst transcriptional activity influences kirre mRNA concentration in the Drosophila pupal retina during the final steps of ommatidial patterning.Maiaro Cabral Rosa MachadoShirlei Octacilio-SilvaMara Silvia A CostaRicardo Guelerman P Ramos<h4>Background</h4>Drosophila retinal architecture is laid down between 24-48 hours after puparium formation, when some of the still uncommitted interommatidial cells (IOCs) are recruited to become secondary and tertiary pigment cells while the remaining ones undergo apoptosis. This choice between survival and death requires the product of the roughest (rst) gene, an immunoglobulin superfamily transmembrane glycoprotein involved in a wide range of developmental processes. Both temporal misexpression of Rst and truncation of the protein intracytoplasmic domain, lead to severe defects in which IOCs either remain mostly undifferentiated and die late and erratically or, instead, differentiate into extra pigment cells. Intriguingly, mutants not expressing wild type protein often have normal or very mild rough eyes.<h4>Methodology/principal findings</h4>By using quantitative real time PCR to examine rst transcriptional dynamics in the pupal retina, both in wild type and mutant alleles we showed that tightly regulated temporal changes in rst transcriptional rate underlie its proper function during the final steps of eye patterning. Furthermore we demonstrated that the unexpected wild type eye phenotype of mutants with low or no rst expression correlates with an upregulation in the mRNA levels of the rst paralogue kin-of-irre (kirre), which seems able to substitute for rst function in this process, similarly to their role in myoblast fusion. This compensatory upregulation of kirre mRNA levels could be directly induced in wild type pupa upon RNAi-mediated silencing of rst, indicating that expression of both genes is also coordinately regulated in physiological conditions.<h4>Conclusions/significance</h4>These findings suggest a general mechanism by which rst and kirre expression could be fine tuned to optimize their redundant roles during development and provide a clearer picture of how the specification of survival and apoptotic fates by differential cell adhesion during the final steps of retinal morphogenesis in insects are controlled at the transcriptional level.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21857931/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Maiaro Cabral Rosa Machado
Shirlei Octacilio-Silva
Mara Silvia A Costa
Ricardo Guelerman P Ramos
spellingShingle Maiaro Cabral Rosa Machado
Shirlei Octacilio-Silva
Mara Silvia A Costa
Ricardo Guelerman P Ramos
rst transcriptional activity influences kirre mRNA concentration in the Drosophila pupal retina during the final steps of ommatidial patterning.
PLoS ONE
author_facet Maiaro Cabral Rosa Machado
Shirlei Octacilio-Silva
Mara Silvia A Costa
Ricardo Guelerman P Ramos
author_sort Maiaro Cabral Rosa Machado
title rst transcriptional activity influences kirre mRNA concentration in the Drosophila pupal retina during the final steps of ommatidial patterning.
title_short rst transcriptional activity influences kirre mRNA concentration in the Drosophila pupal retina during the final steps of ommatidial patterning.
title_full rst transcriptional activity influences kirre mRNA concentration in the Drosophila pupal retina during the final steps of ommatidial patterning.
title_fullStr rst transcriptional activity influences kirre mRNA concentration in the Drosophila pupal retina during the final steps of ommatidial patterning.
title_full_unstemmed rst transcriptional activity influences kirre mRNA concentration in the Drosophila pupal retina during the final steps of ommatidial patterning.
title_sort rst transcriptional activity influences kirre mrna concentration in the drosophila pupal retina during the final steps of ommatidial patterning.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2011-01-01
description <h4>Background</h4>Drosophila retinal architecture is laid down between 24-48 hours after puparium formation, when some of the still uncommitted interommatidial cells (IOCs) are recruited to become secondary and tertiary pigment cells while the remaining ones undergo apoptosis. This choice between survival and death requires the product of the roughest (rst) gene, an immunoglobulin superfamily transmembrane glycoprotein involved in a wide range of developmental processes. Both temporal misexpression of Rst and truncation of the protein intracytoplasmic domain, lead to severe defects in which IOCs either remain mostly undifferentiated and die late and erratically or, instead, differentiate into extra pigment cells. Intriguingly, mutants not expressing wild type protein often have normal or very mild rough eyes.<h4>Methodology/principal findings</h4>By using quantitative real time PCR to examine rst transcriptional dynamics in the pupal retina, both in wild type and mutant alleles we showed that tightly regulated temporal changes in rst transcriptional rate underlie its proper function during the final steps of eye patterning. Furthermore we demonstrated that the unexpected wild type eye phenotype of mutants with low or no rst expression correlates with an upregulation in the mRNA levels of the rst paralogue kin-of-irre (kirre), which seems able to substitute for rst function in this process, similarly to their role in myoblast fusion. This compensatory upregulation of kirre mRNA levels could be directly induced in wild type pupa upon RNAi-mediated silencing of rst, indicating that expression of both genes is also coordinately regulated in physiological conditions.<h4>Conclusions/significance</h4>These findings suggest a general mechanism by which rst and kirre expression could be fine tuned to optimize their redundant roles during development and provide a clearer picture of how the specification of survival and apoptotic fates by differential cell adhesion during the final steps of retinal morphogenesis in insects are controlled at the transcriptional level.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21857931/?tool=EBI
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