Mutations in Growth-Related Genes Induced by EMS Treatment in Scallops

Background: The goal of genetic breeding is to select variants with mutations that are related to expected traits, such as fast growth. Artificial induction has been widely used to obtain strains with more mutations for further selection. Ethylmethylsulfone (EMS) is one of the most commonly used che...

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Main Authors: Caihui Wang, Bo Liu, Min Chen, Junhao Ning, Xia Lu, Chunde Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2022.879844/full
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author Caihui Wang
Bo Liu
Min Chen
Junhao Ning
Xia Lu
Chunde Wang
Chunde Wang
author_facet Caihui Wang
Bo Liu
Min Chen
Junhao Ning
Xia Lu
Chunde Wang
Chunde Wang
author_sort Caihui Wang
collection DOAJ
description Background: The goal of genetic breeding is to select variants with mutations that are related to expected traits, such as fast growth. Artificial induction has been widely used to obtain strains with more mutations for further selection. Ethylmethylsulfone (EMS) is one of the most commonly used chemical mutagens in plant and microorganism breeding. However, the application of EMS mutagenesis in shellfish has not been reported. The aim of this study is to evaluate the potential use of EMS as a mutagen in scallop breeding, especially in characterization of mutations in growth-related genes.Results: Our results indicated that hatching of about 50% of fertilized eggs was blocked by treatment with 20 mM EMS for 3 h and the resulted larvae developed normally into adult stages. We then evaluated the mutagenic effects of EMS by sequencing the genomes of 4 adult scallops from the control group and 12 from the treatment group at 8 months after fertilization. On average, after removing shared types of mutations, there were 1,151,380 ± 258,188 SNPs (Single Nucleotide Polymorphisms) and 229,256 ± 51,714 InDels (insertion-deletion) in each animal in the EMS treatment group, while there were only134841 ± 10,115 SNPs and 42,605 ± 5,136 InDels in the control group. The average mutation rate in the genome of the EMS treatment group (0.0137 ± 0.0013%) was about 9 times that of the control group (0.0015 ± 0.0002%). GO (Gene Ontology) annotation and KEGG (Kyoto Encyclopedia of Genes and Genomes) enrichment analyses revealed that mutations induced by EMS occurred evenly in most biological processes, cellular components and functions, as well in most pathways. However, significant lower percentage of mutations were found in the exonic region, in non-synonymous or Stopgain/Stoploss SNPs and in coding domains, suggesting apparent DNA repair or selection during grow-out stage. Analyses of the growth-related genes with mutations indicated that mutations in MFS (Major Facilitator Superfamily) and Tubulin were only found in the large-sized group (Five largest scallops: Treated-1, Treated-2, Treated-3, Treated-4, and Treated-5) and Homeobox and Socs (Suppressor of cytokine signaling) only in the small group (Two smallest scallops: Treated-11 and Treated-12). These results suggested that these genes may be involved in the regulation of growth in these animals, although further verification is certainly warranted.Conclusion: Treatment of fertilized eggs with 20 mM EMS for 3 h induced 9 times more mutations in scallop genomes. We found that mutations in MFS and Tubulin may be related to fast growth in the large-sized group and those mutations in Homeobox and SOCs may be involved in the slow growth in the small-sized scallops. EMS can be used to accelerate selection of economically important traits in molluscs.
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spelling doaj.art-abe5c43470f84b28b0c088adbb9fb3912022-12-22T01:52:51ZengFrontiers Media S.A.Frontiers in Genetics1664-80212022-04-011310.3389/fgene.2022.879844879844Mutations in Growth-Related Genes Induced by EMS Treatment in ScallopsCaihui Wang0Bo Liu1Min Chen2Junhao Ning3Xia Lu4Chunde Wang5Chunde Wang6School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, ChinaSchool of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, ChinaYantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, ChinaYantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, ChinaYantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, ChinaSchool of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, ChinaYantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, ChinaBackground: The goal of genetic breeding is to select variants with mutations that are related to expected traits, such as fast growth. Artificial induction has been widely used to obtain strains with more mutations for further selection. Ethylmethylsulfone (EMS) is one of the most commonly used chemical mutagens in plant and microorganism breeding. However, the application of EMS mutagenesis in shellfish has not been reported. The aim of this study is to evaluate the potential use of EMS as a mutagen in scallop breeding, especially in characterization of mutations in growth-related genes.Results: Our results indicated that hatching of about 50% of fertilized eggs was blocked by treatment with 20 mM EMS for 3 h and the resulted larvae developed normally into adult stages. We then evaluated the mutagenic effects of EMS by sequencing the genomes of 4 adult scallops from the control group and 12 from the treatment group at 8 months after fertilization. On average, after removing shared types of mutations, there were 1,151,380 ± 258,188 SNPs (Single Nucleotide Polymorphisms) and 229,256 ± 51,714 InDels (insertion-deletion) in each animal in the EMS treatment group, while there were only134841 ± 10,115 SNPs and 42,605 ± 5,136 InDels in the control group. The average mutation rate in the genome of the EMS treatment group (0.0137 ± 0.0013%) was about 9 times that of the control group (0.0015 ± 0.0002%). GO (Gene Ontology) annotation and KEGG (Kyoto Encyclopedia of Genes and Genomes) enrichment analyses revealed that mutations induced by EMS occurred evenly in most biological processes, cellular components and functions, as well in most pathways. However, significant lower percentage of mutations were found in the exonic region, in non-synonymous or Stopgain/Stoploss SNPs and in coding domains, suggesting apparent DNA repair or selection during grow-out stage. Analyses of the growth-related genes with mutations indicated that mutations in MFS (Major Facilitator Superfamily) and Tubulin were only found in the large-sized group (Five largest scallops: Treated-1, Treated-2, Treated-3, Treated-4, and Treated-5) and Homeobox and Socs (Suppressor of cytokine signaling) only in the small group (Two smallest scallops: Treated-11 and Treated-12). These results suggested that these genes may be involved in the regulation of growth in these animals, although further verification is certainly warranted.Conclusion: Treatment of fertilized eggs with 20 mM EMS for 3 h induced 9 times more mutations in scallop genomes. We found that mutations in MFS and Tubulin may be related to fast growth in the large-sized group and those mutations in Homeobox and SOCs may be involved in the slow growth in the small-sized scallops. EMS can be used to accelerate selection of economically important traits in molluscs.https://www.frontiersin.org/articles/10.3389/fgene.2022.879844/fullEMSmutagenscallopgenome sequencingSNPINDEL
spellingShingle Caihui Wang
Bo Liu
Min Chen
Junhao Ning
Xia Lu
Chunde Wang
Chunde Wang
Mutations in Growth-Related Genes Induced by EMS Treatment in Scallops
Frontiers in Genetics
EMS
mutagen
scallop
genome sequencing
SNP
INDEL
title Mutations in Growth-Related Genes Induced by EMS Treatment in Scallops
title_full Mutations in Growth-Related Genes Induced by EMS Treatment in Scallops
title_fullStr Mutations in Growth-Related Genes Induced by EMS Treatment in Scallops
title_full_unstemmed Mutations in Growth-Related Genes Induced by EMS Treatment in Scallops
title_short Mutations in Growth-Related Genes Induced by EMS Treatment in Scallops
title_sort mutations in growth related genes induced by ems treatment in scallops
topic EMS
mutagen
scallop
genome sequencing
SNP
INDEL
url https://www.frontiersin.org/articles/10.3389/fgene.2022.879844/full
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AT xialu mutationsingrowthrelatedgenesinducedbyemstreatmentinscallops
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