Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks

Abstract Hox genes are key developmental regulators that are involved in establishing morphological features during animal ontogeny. They are commonly expressed along the anterior–posterior axis in a staggered, or collinear, fashion. In mollusks, the repertoire of body plans is widely diverse and cu...

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Autores principales: David A. Salamanca-Díaz, Andrew D. Calcino, André L. de Oliveira, Andreas Wanninger
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Publicado: Nature Portfolio 2021
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spelling oai:doaj.org-article:7830ab2e9ac5481bba2cd59135cca6622021-12-02T13:30:27ZNon-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks10.1038/s41598-021-82122-62045-2322https://doaj.org/article/7830ab2e9ac5481bba2cd59135cca6622021-02-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-82122-6https://doaj.org/toc/2045-2322Abstract Hox genes are key developmental regulators that are involved in establishing morphological features during animal ontogeny. They are commonly expressed along the anterior–posterior axis in a staggered, or collinear, fashion. In mollusks, the repertoire of body plans is widely diverse and current data suggest their involvement during development of landmark morphological traits in Conchifera, one of the two major lineages that comprises those taxa that originated from a uni-shelled ancestor (Monoplacophora, Gastropoda, Cephalopoda, Scaphopoda, Bivalvia). For most clades, and bivalves in particular, data on Hox gene expression throughout ontogeny are scarce. We thus investigated Hox expression during development of the quagga mussel, Dreissena rostriformis, to elucidate to which degree they might contribute to specific phenotypic traits as in other conchiferans. The Hox/ParaHox complement of Mollusca typically comprises 14 genes, 13 of which are present in bivalve genomes including Dreissena. We describe here expression of 9 Hox genes and the ParaHox gene Xlox during Dreissena development. Hox expression in Dreissena is first detected in the gastrula stage with widely overlapping expression domains of most genes. In the trochophore stage, Hox gene expression shifts towards more compact, largely mesodermal domains. Only few of these domains can be assigned to specific developing morphological structures such as Hox1 in the shell field and Xlox in the hindgut. We did not find traces of spatial or temporal staggered expression of Hox genes in Dreissena. Our data support the notion that Hox gene expression has been coopted independently, and to varying degrees, into lineage-specific structures in the respective conchiferan clades. The non-collinear mode of Hox expression in Dreissena might be a result of the low degree of body plan regionalization along the bivalve anterior–posterior axis as exemplified by the lack of key morphological traits such as a distinct head, cephalic tentacles, radula apparatus, and a simplified central nervous system.David A. Salamanca-DíazAndrew D. CalcinoAndré L. de OliveiraAndreas WanningerNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-12 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
David A. Salamanca-Díaz
Andrew D. Calcino
André L. de Oliveira
Andreas Wanninger
Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks
description Abstract Hox genes are key developmental regulators that are involved in establishing morphological features during animal ontogeny. They are commonly expressed along the anterior–posterior axis in a staggered, or collinear, fashion. In mollusks, the repertoire of body plans is widely diverse and current data suggest their involvement during development of landmark morphological traits in Conchifera, one of the two major lineages that comprises those taxa that originated from a uni-shelled ancestor (Monoplacophora, Gastropoda, Cephalopoda, Scaphopoda, Bivalvia). For most clades, and bivalves in particular, data on Hox gene expression throughout ontogeny are scarce. We thus investigated Hox expression during development of the quagga mussel, Dreissena rostriformis, to elucidate to which degree they might contribute to specific phenotypic traits as in other conchiferans. The Hox/ParaHox complement of Mollusca typically comprises 14 genes, 13 of which are present in bivalve genomes including Dreissena. We describe here expression of 9 Hox genes and the ParaHox gene Xlox during Dreissena development. Hox expression in Dreissena is first detected in the gastrula stage with widely overlapping expression domains of most genes. In the trochophore stage, Hox gene expression shifts towards more compact, largely mesodermal domains. Only few of these domains can be assigned to specific developing morphological structures such as Hox1 in the shell field and Xlox in the hindgut. We did not find traces of spatial or temporal staggered expression of Hox genes in Dreissena. Our data support the notion that Hox gene expression has been coopted independently, and to varying degrees, into lineage-specific structures in the respective conchiferan clades. The non-collinear mode of Hox expression in Dreissena might be a result of the low degree of body plan regionalization along the bivalve anterior–posterior axis as exemplified by the lack of key morphological traits such as a distinct head, cephalic tentacles, radula apparatus, and a simplified central nervous system.
format article
author David A. Salamanca-Díaz
Andrew D. Calcino
André L. de Oliveira
Andreas Wanninger
author_facet David A. Salamanca-Díaz
Andrew D. Calcino
André L. de Oliveira
Andreas Wanninger
author_sort David A. Salamanca-Díaz
title Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks
title_short Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks
title_full Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks
title_fullStr Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks
title_full_unstemmed Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks
title_sort non-collinear hox gene expression in bivalves and the evolution of morphological novelties in mollusks
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/7830ab2e9ac5481bba2cd59135cca662
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AT andreldeoliveira noncollinearhoxgeneexpressioninbivalvesandtheevolutionofmorphologicalnoveltiesinmollusks
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