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Alteration of synonymous codon usage bias accompanies polyploidization in wheat

The diploidization of polyploid genomes is accompanied by genomic variation, including synonymous nucleotide substitutions that may lead to synonymous codon usage bias (SCUB). SCUB can mirror the evolutionary specialization of plants, but its effect on the formation of polyploidies is not well docum...

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Autores principales: Tian, Geng, Xiao, Guilian, Wu, Tong, Zhou, Junzhi, Xu, Wenjing, Wang, Yanxia, Xia, Guangmin, Wang, Mengcheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9614214/
https://www.ncbi.nlm.nih.gov/pubmed/36313462
http://dx.doi.org/10.3389/fgene.2022.979902
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author Tian, Geng
Xiao, Guilian
Wu, Tong
Zhou, Junzhi
Xu, Wenjing
Wang, Yanxia
Xia, Guangmin
Wang, Mengcheng
author_facet Tian, Geng
Xiao, Guilian
Wu, Tong
Zhou, Junzhi
Xu, Wenjing
Wang, Yanxia
Xia, Guangmin
Wang, Mengcheng
author_sort Tian, Geng
collection PubMed
description The diploidization of polyploid genomes is accompanied by genomic variation, including synonymous nucleotide substitutions that may lead to synonymous codon usage bias (SCUB). SCUB can mirror the evolutionary specialization of plants, but its effect on the formation of polyploidies is not well documented. We explored this issue here with hexaploid wheat and its progenitors. Synonymous codons (SCs) ending in either cytosine (NNC) or guanidine (NNG) were more frequent than those ending in either adenosine (NNA) or thymine (NNT), and the preference for NNC/G codons followed the increase in genome ploidy. The ratios between NNC/G and NNA/T codons gradually decreased in genes with more introns, and the difference in these ratios between wheat and its progenitors diminished with increasing ploidy. SCUB frequencies were heterogeneous among exons, and the bias preferred to NNA/T in more internal exons, especially for genes with more exons; while the preference did not appear to associate with ploidy. The SCUB alteration of the progenitors was different during the formation of hexaploid wheat, so that SCUB was the homogeneous among A, B and D subgenomes. DNA methylation-mediated conversion from cytosine to thymine weakened following the increase of genome ploidy, coinciding with the stronger bias for NNC/G SCs in the genome as a function of ploidy, suggesting that SCUB contribute to the epigenetic variation in hexaploid wheat. The patterns in SCUB mirrored the formation of hexaploid wheat, which provides new insight into genome shock-induced genetic variation during polyploidization. SCs representing non-neutral synonymous mutations can be used for genetic dissection and improvement of agricultural traits of wheat and other polyploidies.
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spelling pubmed-96142142022-10-29 Alteration of synonymous codon usage bias accompanies polyploidization in wheat Tian, Geng Xiao, Guilian Wu, Tong Zhou, Junzhi Xu, Wenjing Wang, Yanxia Xia, Guangmin Wang, Mengcheng Front Genet Genetics The diploidization of polyploid genomes is accompanied by genomic variation, including synonymous nucleotide substitutions that may lead to synonymous codon usage bias (SCUB). SCUB can mirror the evolutionary specialization of plants, but its effect on the formation of polyploidies is not well documented. We explored this issue here with hexaploid wheat and its progenitors. Synonymous codons (SCs) ending in either cytosine (NNC) or guanidine (NNG) were more frequent than those ending in either adenosine (NNA) or thymine (NNT), and the preference for NNC/G codons followed the increase in genome ploidy. The ratios between NNC/G and NNA/T codons gradually decreased in genes with more introns, and the difference in these ratios between wheat and its progenitors diminished with increasing ploidy. SCUB frequencies were heterogeneous among exons, and the bias preferred to NNA/T in more internal exons, especially for genes with more exons; while the preference did not appear to associate with ploidy. The SCUB alteration of the progenitors was different during the formation of hexaploid wheat, so that SCUB was the homogeneous among A, B and D subgenomes. DNA methylation-mediated conversion from cytosine to thymine weakened following the increase of genome ploidy, coinciding with the stronger bias for NNC/G SCs in the genome as a function of ploidy, suggesting that SCUB contribute to the epigenetic variation in hexaploid wheat. The patterns in SCUB mirrored the formation of hexaploid wheat, which provides new insight into genome shock-induced genetic variation during polyploidization. SCs representing non-neutral synonymous mutations can be used for genetic dissection and improvement of agricultural traits of wheat and other polyploidies. Frontiers Media S.A. 2022-10-14 /pmc/articles/PMC9614214/ /pubmed/36313462 http://dx.doi.org/10.3389/fgene.2022.979902 Text en Copyright © 2022 Tian, Xiao, Wu, Zhou, Xu, Wang, Xia and Wang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Genetics
Tian, Geng
Xiao, Guilian
Wu, Tong
Zhou, Junzhi
Xu, Wenjing
Wang, Yanxia
Xia, Guangmin
Wang, Mengcheng
Alteration of synonymous codon usage bias accompanies polyploidization in wheat
title Alteration of synonymous codon usage bias accompanies polyploidization in wheat
title_full Alteration of synonymous codon usage bias accompanies polyploidization in wheat
title_fullStr Alteration of synonymous codon usage bias accompanies polyploidization in wheat
title_full_unstemmed Alteration of synonymous codon usage bias accompanies polyploidization in wheat
title_short Alteration of synonymous codon usage bias accompanies polyploidization in wheat
title_sort alteration of synonymous codon usage bias accompanies polyploidization in wheat
topic Genetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9614214/
https://www.ncbi.nlm.nih.gov/pubmed/36313462
http://dx.doi.org/10.3389/fgene.2022.979902
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