Functional Divergence of the <i>Tribolium castaneum engrailed</i> and <i>invected</i> Paralogs

<i>Engrailed (en)</i> and <i>invected (inv)</i> encode paralogous transcription factors found as a closely linked tandem duplication within holometabolous insects. <i>Drosophila en</i> mutants segment normally, then fail to maintain their segments. Loss of <i&g...

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Main Authors: Summer Blunk, Hector Garcia-Verdugo, Sierra O’Sullivan, James Camp, Michael Haines, Tara Coalter, Terri A. Williams, Lisa M. Nagy
Format: Article
Language:English
Published: MDPI AG 2023-08-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/14/8/691
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author Summer Blunk
Hector Garcia-Verdugo
Sierra O’Sullivan
James Camp
Michael Haines
Tara Coalter
Terri A. Williams
Lisa M. Nagy
author_facet Summer Blunk
Hector Garcia-Verdugo
Sierra O’Sullivan
James Camp
Michael Haines
Tara Coalter
Terri A. Williams
Lisa M. Nagy
author_sort Summer Blunk
collection DOAJ
description <i>Engrailed (en)</i> and <i>invected (inv)</i> encode paralogous transcription factors found as a closely linked tandem duplication within holometabolous insects. <i>Drosophila en</i> mutants segment normally, then fail to maintain their segments. Loss of <i>Drosophila inv</i> is viable, while loss of both genes results in asegmental larvae. Surprisingly, the knockdown of <i>Oncopeltus inv</i> can result in the loss or fusion of the entire abdomen and <i>en</i> knockdowns in <i>Tribolium</i> show variable degrees of segmental loss. The consequence of losing or knocking down both paralogs on embryogenesis has not been studied beyond <i>Drosophila</i>. To further investigate the relative functions of each paralog and the mechanism behind the segmental loss, <i>Tribolium</i> double and single knockdowns of <i>en</i> and <i>inv</i> were analyzed. The most common cuticular phenotype of the double knockdowns was small, limbless, and open dorsally, with all but a single, segmentally iterated row of bristles. Less severe knockdowns had fused segments and reduced appendages. The <i>Tribolium</i> paralogs appear to act synergistically: the knockdown of either <i>Tribolium</i> gene alone was typically less severe, with all limbs present, whereas the most extreme single knockdowns mimic the most severe double knockdown phenotype. Morphological abnormalities unique to either single gene knockdown were not found. <i>inv</i> expression was not affected in the <i>Tribolium en</i> knockdowns, but <i>hh</i> expression was unexpectedly increased midway through development. Thus, while the segmental expression of <i>en/inv</i> is broadly conserved within insects, the functions of <i>en</i> and <i>inv</i> are evolving independently in different lineages.
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spelling doaj.art-ef116d5cc557441dbb7238c51bc3a6b42023-11-19T01:36:36ZengMDPI AGInsects2075-44502023-08-0114869110.3390/insects14080691Functional Divergence of the <i>Tribolium castaneum engrailed</i> and <i>invected</i> ParalogsSummer Blunk0Hector Garcia-Verdugo1Sierra O’Sullivan2James Camp3Michael Haines4Tara Coalter5Terri A. Williams6Lisa M. Nagy7Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USAMolecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USAMolecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USABiology Department, Trinity College, Hartford, CT 06106, USAMolecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USAMolecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USABiology Department, Trinity College, Hartford, CT 06106, USAMolecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USA<i>Engrailed (en)</i> and <i>invected (inv)</i> encode paralogous transcription factors found as a closely linked tandem duplication within holometabolous insects. <i>Drosophila en</i> mutants segment normally, then fail to maintain their segments. Loss of <i>Drosophila inv</i> is viable, while loss of both genes results in asegmental larvae. Surprisingly, the knockdown of <i>Oncopeltus inv</i> can result in the loss or fusion of the entire abdomen and <i>en</i> knockdowns in <i>Tribolium</i> show variable degrees of segmental loss. The consequence of losing or knocking down both paralogs on embryogenesis has not been studied beyond <i>Drosophila</i>. To further investigate the relative functions of each paralog and the mechanism behind the segmental loss, <i>Tribolium</i> double and single knockdowns of <i>en</i> and <i>inv</i> were analyzed. The most common cuticular phenotype of the double knockdowns was small, limbless, and open dorsally, with all but a single, segmentally iterated row of bristles. Less severe knockdowns had fused segments and reduced appendages. The <i>Tribolium</i> paralogs appear to act synergistically: the knockdown of either <i>Tribolium</i> gene alone was typically less severe, with all limbs present, whereas the most extreme single knockdowns mimic the most severe double knockdown phenotype. Morphological abnormalities unique to either single gene knockdown were not found. <i>inv</i> expression was not affected in the <i>Tribolium en</i> knockdowns, but <i>hh</i> expression was unexpectedly increased midway through development. Thus, while the segmental expression of <i>en/inv</i> is broadly conserved within insects, the functions of <i>en</i> and <i>inv</i> are evolving independently in different lineages.https://www.mdpi.com/2075-4450/14/8/691<i>engrailed</i>invectedsegment-polaritysequential segmentation<i>Tribolium</i>gene paralogs
spellingShingle Summer Blunk
Hector Garcia-Verdugo
Sierra O’Sullivan
James Camp
Michael Haines
Tara Coalter
Terri A. Williams
Lisa M. Nagy
Functional Divergence of the <i>Tribolium castaneum engrailed</i> and <i>invected</i> Paralogs
Insects
<i>engrailed</i>
invected
segment-polarity
sequential segmentation
<i>Tribolium</i>
gene paralogs
title Functional Divergence of the <i>Tribolium castaneum engrailed</i> and <i>invected</i> Paralogs
title_full Functional Divergence of the <i>Tribolium castaneum engrailed</i> and <i>invected</i> Paralogs
title_fullStr Functional Divergence of the <i>Tribolium castaneum engrailed</i> and <i>invected</i> Paralogs
title_full_unstemmed Functional Divergence of the <i>Tribolium castaneum engrailed</i> and <i>invected</i> Paralogs
title_short Functional Divergence of the <i>Tribolium castaneum engrailed</i> and <i>invected</i> Paralogs
title_sort functional divergence of the i tribolium castaneum engrailed i and i invected i paralogs
topic <i>engrailed</i>
invected
segment-polarity
sequential segmentation
<i>Tribolium</i>
gene paralogs
url https://www.mdpi.com/2075-4450/14/8/691
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