Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of Monotremes

Chromosome segregation at mitosis and meiosis is a highly dynamic and tightly regulated process that involves a large number of components. Due to the fundamental nature of chromosome segregation, many genes involved in this process are evolutionarily highly conserved, but duplications and functiona...

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Main Authors: Filip Pajpach, Linda Shearwin-Whyatt, Frank Grützner
Format: Article
Language:English
Published: MDPI AG 2021-08-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/12/9/1320
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spelling doaj-31bfd48cfbbf423083b00ff01331a54b2021-09-26T00:12:57ZengMDPI AGGenes2073-44252021-08-01121320132010.3390/genes12091320Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of MonotremesFilip Pajpach0Linda Shearwin-Whyatt1Frank Grützner2School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, AustraliaSchool of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, AustraliaSchool of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, AustraliaChromosome segregation at mitosis and meiosis is a highly dynamic and tightly regulated process that involves a large number of components. Due to the fundamental nature of chromosome segregation, many genes involved in this process are evolutionarily highly conserved, but duplications and functional diversification has occurred in various lineages. In order to better understand the evolution of genes involved in chromosome segregation in mammals, we analyzed some of the key components in the basal mammalian lineage of egg-laying mammals. The chromosome passenger complex is a multiprotein complex central to chromosome segregation during both mitosis and meiosis. It consists of survivin, borealin, inner centromere protein, and Aurora kinase B or C. We confirm the absence of Aurora kinase C in marsupials and show its absence in both platypus and echidna, which supports the current model of the evolution of Aurora kinases. High expression of <i>AURKBC</i>, an ancestor of <i>AURKB</i> and <i>AURKC</i> present in monotremes, suggests that this gene is performing all necessary meiotic functions in monotremes. Other genes of the chromosome passenger complex complex are present and conserved in monotremes, suggesting that their function has been preserved in mammals. Cohesins are another family of genes that are of vital importance for chromosome cohesion and segregation at mitosis and meiosis. Previous work has demonstrated an accumulation and differential loading of structural maintenance of chromosomes 3 (SMC3) on the platypus sex chromosome complex at meiotic prophase I. We investigated if a similar accumulation occurs in the echidna during meiosis I. In contrast to platypus, SMC3 was only found on the synaptonemal complex in echidna. This indicates that the specific distribution of SMC3 on the sex chromosome complex may have evolved specifically in platypus.https://www.mdpi.com/2073-4425/12/9/1320Aurora kinasechromosome passenger complexcohesinmonotrememeiosissex chromosome multiple
collection DOAJ
language English
format Article
sources DOAJ
author Filip Pajpach
Linda Shearwin-Whyatt
Frank Grützner
spellingShingle Filip Pajpach
Linda Shearwin-Whyatt
Frank Grützner
Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of Monotremes
Genes
Aurora kinase
chromosome passenger complex
cohesin
monotreme
meiosis
sex chromosome multiple
author_facet Filip Pajpach
Linda Shearwin-Whyatt
Frank Grützner
author_sort Filip Pajpach
title Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of Monotremes
title_short Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of Monotremes
title_full Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of Monotremes
title_fullStr Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of Monotremes
title_full_unstemmed Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of Monotremes
title_sort evolution, expression and meiotic behavior of genes involved in chromosome segregation of monotremes
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2021-08-01
description Chromosome segregation at mitosis and meiosis is a highly dynamic and tightly regulated process that involves a large number of components. Due to the fundamental nature of chromosome segregation, many genes involved in this process are evolutionarily highly conserved, but duplications and functional diversification has occurred in various lineages. In order to better understand the evolution of genes involved in chromosome segregation in mammals, we analyzed some of the key components in the basal mammalian lineage of egg-laying mammals. The chromosome passenger complex is a multiprotein complex central to chromosome segregation during both mitosis and meiosis. It consists of survivin, borealin, inner centromere protein, and Aurora kinase B or C. We confirm the absence of Aurora kinase C in marsupials and show its absence in both platypus and echidna, which supports the current model of the evolution of Aurora kinases. High expression of <i>AURKBC</i>, an ancestor of <i>AURKB</i> and <i>AURKC</i> present in monotremes, suggests that this gene is performing all necessary meiotic functions in monotremes. Other genes of the chromosome passenger complex complex are present and conserved in monotremes, suggesting that their function has been preserved in mammals. Cohesins are another family of genes that are of vital importance for chromosome cohesion and segregation at mitosis and meiosis. Previous work has demonstrated an accumulation and differential loading of structural maintenance of chromosomes 3 (SMC3) on the platypus sex chromosome complex at meiotic prophase I. We investigated if a similar accumulation occurs in the echidna during meiosis I. In contrast to platypus, SMC3 was only found on the synaptonemal complex in echidna. This indicates that the specific distribution of SMC3 on the sex chromosome complex may have evolved specifically in platypus.
topic Aurora kinase
chromosome passenger complex
cohesin
monotreme
meiosis
sex chromosome multiple
url https://www.mdpi.com/2073-4425/12/9/1320
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