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The Shift in Synonymous Codon Usage Reveals Similar Genomic Variation during Domestication of Asian and African Rice

The domestication of wild rice occurred together with genomic variation, including the synonymous nucleotide substitutions that result in synonymous codon usage bias (SCUB). SCUB mirrors the evolutionary specialization of plants, but its characteristics during domestication were not yet addressed. H...

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Autores principales: Xiao, Guilian, Zhou, Junzhi, Huo, Zhiheng, Wu, Tong, Li, Yingchun, Li, Yajing, Wang, Yanxia, Wang, Mengcheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9656316/
https://www.ncbi.nlm.nih.gov/pubmed/36361651
http://dx.doi.org/10.3390/ijms232112860
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author Xiao, Guilian
Zhou, Junzhi
Huo, Zhiheng
Wu, Tong
Li, Yingchun
Li, Yajing
Wang, Yanxia
Wang, Mengcheng
author_facet Xiao, Guilian
Zhou, Junzhi
Huo, Zhiheng
Wu, Tong
Li, Yingchun
Li, Yajing
Wang, Yanxia
Wang, Mengcheng
author_sort Xiao, Guilian
collection PubMed
description The domestication of wild rice occurred together with genomic variation, including the synonymous nucleotide substitutions that result in synonymous codon usage bias (SCUB). SCUB mirrors the evolutionary specialization of plants, but its characteristics during domestication were not yet addressed. Here, we found cytosine- and guanidine-ending (NNC and NNG) synonymous codons (SCs) were more pronounced than adenosine- and thymine-ending SCs (NNA and NNT) in both wild and cultivated species of Asian and African rice. The ratios of NNC/G to NNA/T codons gradually decreased following the rise in the number of introns, and the preference for NNA/T codons became more obvious in genes with more introns in cultivated rice when compared with those in wild rice. SCUB frequencies were heterogeneous across the exons, with a higher preference for NNA/T in internal exons than in terminal exons. The preference for NNA/T in internal but not terminal exons was more predominant in cultivated rice than in wild rice, with the difference between wild and cultivated rice becoming more remarkable with the rise in exon numbers. The difference in the ratios of codon combinations representing DNA methylation-mediated conversion from cytosine to thymine between wild and cultivated rice coincided with their difference in SCUB frequencies, suggesting that SCUB reveals the possible association between genetic and epigenetic variation during the domestication of rice. Similar patterns of SCUB shift in Asian and African rice indicate that genomic variation occurs in the same non-random manner. SCUB representing non-neutral synonymous mutations can provide insight into the mechanism of genomic variation in domestication and can be used for the genetic dissection of agricultural traits in rice and other crops.
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spelling pubmed-96563162022-11-15 The Shift in Synonymous Codon Usage Reveals Similar Genomic Variation during Domestication of Asian and African Rice Xiao, Guilian Zhou, Junzhi Huo, Zhiheng Wu, Tong Li, Yingchun Li, Yajing Wang, Yanxia Wang, Mengcheng Int J Mol Sci Article The domestication of wild rice occurred together with genomic variation, including the synonymous nucleotide substitutions that result in synonymous codon usage bias (SCUB). SCUB mirrors the evolutionary specialization of plants, but its characteristics during domestication were not yet addressed. Here, we found cytosine- and guanidine-ending (NNC and NNG) synonymous codons (SCs) were more pronounced than adenosine- and thymine-ending SCs (NNA and NNT) in both wild and cultivated species of Asian and African rice. The ratios of NNC/G to NNA/T codons gradually decreased following the rise in the number of introns, and the preference for NNA/T codons became more obvious in genes with more introns in cultivated rice when compared with those in wild rice. SCUB frequencies were heterogeneous across the exons, with a higher preference for NNA/T in internal exons than in terminal exons. The preference for NNA/T in internal but not terminal exons was more predominant in cultivated rice than in wild rice, with the difference between wild and cultivated rice becoming more remarkable with the rise in exon numbers. The difference in the ratios of codon combinations representing DNA methylation-mediated conversion from cytosine to thymine between wild and cultivated rice coincided with their difference in SCUB frequencies, suggesting that SCUB reveals the possible association between genetic and epigenetic variation during the domestication of rice. Similar patterns of SCUB shift in Asian and African rice indicate that genomic variation occurs in the same non-random manner. SCUB representing non-neutral synonymous mutations can provide insight into the mechanism of genomic variation in domestication and can be used for the genetic dissection of agricultural traits in rice and other crops. MDPI 2022-10-25 /pmc/articles/PMC9656316/ /pubmed/36361651 http://dx.doi.org/10.3390/ijms232112860 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Xiao, Guilian
Zhou, Junzhi
Huo, Zhiheng
Wu, Tong
Li, Yingchun
Li, Yajing
Wang, Yanxia
Wang, Mengcheng
The Shift in Synonymous Codon Usage Reveals Similar Genomic Variation during Domestication of Asian and African Rice
title The Shift in Synonymous Codon Usage Reveals Similar Genomic Variation during Domestication of Asian and African Rice
title_full The Shift in Synonymous Codon Usage Reveals Similar Genomic Variation during Domestication of Asian and African Rice
title_fullStr The Shift in Synonymous Codon Usage Reveals Similar Genomic Variation during Domestication of Asian and African Rice
title_full_unstemmed The Shift in Synonymous Codon Usage Reveals Similar Genomic Variation during Domestication of Asian and African Rice
title_short The Shift in Synonymous Codon Usage Reveals Similar Genomic Variation during Domestication of Asian and African Rice
title_sort shift in synonymous codon usage reveals similar genomic variation during domestication of asian and african rice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9656316/
https://www.ncbi.nlm.nih.gov/pubmed/36361651
http://dx.doi.org/10.3390/ijms232112860
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