Comparison and Characterization of Phenotypic and Genomic Mutations Induced by a Carbon-Ion Beam and Gamma-ray Irradiation in Soybean (<i>Glycine max</i> (L.) Merr.)

Soybean (<i>Glycine max</i> (L.) Merr.) is a nutritious crop that can provide both oil and protein. A variety of mutagenesis methods have been proposed to obtain better soybean germplasm resources. Among the different types of physical mutagens, carbon-ion beams are considered to be high...

Full description

Bibliographic Details
Main Authors: Zhuo Feng, Yan Du, Jingmin Chen, Xia Chen, Weibin Ren, Lulu Wang, Libin Zhou
Format: Article
Language:English
Published: MDPI AG 2023-05-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/10/8825
_version_ 1797599828706852864
author Zhuo Feng
Yan Du
Jingmin Chen
Xia Chen
Weibin Ren
Lulu Wang
Libin Zhou
author_facet Zhuo Feng
Yan Du
Jingmin Chen
Xia Chen
Weibin Ren
Lulu Wang
Libin Zhou
author_sort Zhuo Feng
collection DOAJ
description Soybean (<i>Glycine max</i> (L.) Merr.) is a nutritious crop that can provide both oil and protein. A variety of mutagenesis methods have been proposed to obtain better soybean germplasm resources. Among the different types of physical mutagens, carbon-ion beams are considered to be highly efficient with high linear energy transfer (LET), and gamma rays have also been widely used for mutation breeding. However, systematic knowledge of the mutagenic effects of these two mutagens during development and on phenotypic and genomic mutations has not yet been elucidated in soybean. To this end, dry seeds of Williams 82 soybean were irradiated with a carbon-ion beam and gamma rays. The biological effects of the M<sub>1</sub> generation included changes in survival rate, yield and fertility. Compared with gamma rays, the relative biological effectiveness (RBE) of the carbon-ion beams was between 2.5 and 3.0. Furthermore, the optimal dose for soybean was determined to be 101 Gy to 115 Gy when using the carbon-ion beam, and it was 263 Gy to 343 Gy when using gamma rays. A total of 325 screened mutant families were detected from out of 2000 M<sub>2</sub> families using the carbon-ion beam, and 336 screened mutant families were found using gamma rays. Regarding the screened phenotypic M<sub>2</sub> mutations, the proportion of low-frequency phenotypic mutations was 23.4% when using a carbon ion beam, and the proportion was 9.8% when using gamma rays. Low-frequency phenotypic mutations were easily obtained with the carbon-ion beam. After screening the mutations from the M<sub>2</sub> generation, their stability was verified, and the genome mutation spectrum of M<sub>3</sub> was systemically profiled. A variety of mutations, including single-base substitutions (SBSs), insertion–deletion mutations (INDELs), multinucleotide variants (MNVs) and structural variants (SVs) were detected with both carbon-ion beam irradiation and gamma-ray irradiation. Overall, 1988 homozygous mutations and 9695 homozygous + heterozygous genotype mutations were detected when using the carbon-ion beam. Additionally, 5279 homozygous mutations and 14,243 homozygous + heterozygous genotype mutations were detected when using gamma rays. The carbon-ion beam, which resulted in low levels of background mutations, has the potential to alleviate the problems caused by linkage drag in soybean mutation breeding. Regarding the genomic mutations, when using the carbon-ion beam, the proportion of homozygous-genotype SVs was 0.45%, and that of homozygous + heterozygous-genotype SVs was 6.27%; meanwhile, the proportions were 0.04% and 4.04% when using gamma rays. A higher proportion of SVs were detected when using the carbon ion beam. The gene effects of missense mutations were greater under carbon-ion beam irradiation, and the gene effects of nonsense mutations were greater under gamma-ray irradiation, which meant that the changes in the amino acid sequences were different between the carbon-ion beam and gamma rays. Taken together, our results demonstrate that both carbon-ion beam and gamma rays are effective techniques for rapid mutation breeding in soybean. If one would like to obtain mutations with a low-frequency phenotype, low levels of background genomic mutations and mutations with a higher proportion of SVs, carbon-ion beams are the best choice.
first_indexed 2024-03-11T03:39:52Z
format Article
id doaj.art-b2c68f411c0d4e879dca75844f13f73c
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-11T03:39:52Z
publishDate 2023-05-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-b2c68f411c0d4e879dca75844f13f73c2023-11-18T01:42:39ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-05-012410882510.3390/ijms24108825Comparison and Characterization of Phenotypic and Genomic Mutations Induced by a Carbon-Ion Beam and Gamma-ray Irradiation in Soybean (<i>Glycine max</i> (L.) Merr.)Zhuo Feng0Yan Du1Jingmin Chen2Xia Chen3Weibin Ren4Lulu Wang5Libin Zhou6Biophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou 730000, ChinaBiophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou 730000, ChinaBiophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou 730000, ChinaBiophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou 730000, ChinaBiophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou 730000, ChinaBiophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou 730000, ChinaBiophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou 730000, ChinaSoybean (<i>Glycine max</i> (L.) Merr.) is a nutritious crop that can provide both oil and protein. A variety of mutagenesis methods have been proposed to obtain better soybean germplasm resources. Among the different types of physical mutagens, carbon-ion beams are considered to be highly efficient with high linear energy transfer (LET), and gamma rays have also been widely used for mutation breeding. However, systematic knowledge of the mutagenic effects of these two mutagens during development and on phenotypic and genomic mutations has not yet been elucidated in soybean. To this end, dry seeds of Williams 82 soybean were irradiated with a carbon-ion beam and gamma rays. The biological effects of the M<sub>1</sub> generation included changes in survival rate, yield and fertility. Compared with gamma rays, the relative biological effectiveness (RBE) of the carbon-ion beams was between 2.5 and 3.0. Furthermore, the optimal dose for soybean was determined to be 101 Gy to 115 Gy when using the carbon-ion beam, and it was 263 Gy to 343 Gy when using gamma rays. A total of 325 screened mutant families were detected from out of 2000 M<sub>2</sub> families using the carbon-ion beam, and 336 screened mutant families were found using gamma rays. Regarding the screened phenotypic M<sub>2</sub> mutations, the proportion of low-frequency phenotypic mutations was 23.4% when using a carbon ion beam, and the proportion was 9.8% when using gamma rays. Low-frequency phenotypic mutations were easily obtained with the carbon-ion beam. After screening the mutations from the M<sub>2</sub> generation, their stability was verified, and the genome mutation spectrum of M<sub>3</sub> was systemically profiled. A variety of mutations, including single-base substitutions (SBSs), insertion–deletion mutations (INDELs), multinucleotide variants (MNVs) and structural variants (SVs) were detected with both carbon-ion beam irradiation and gamma-ray irradiation. Overall, 1988 homozygous mutations and 9695 homozygous + heterozygous genotype mutations were detected when using the carbon-ion beam. Additionally, 5279 homozygous mutations and 14,243 homozygous + heterozygous genotype mutations were detected when using gamma rays. The carbon-ion beam, which resulted in low levels of background mutations, has the potential to alleviate the problems caused by linkage drag in soybean mutation breeding. Regarding the genomic mutations, when using the carbon-ion beam, the proportion of homozygous-genotype SVs was 0.45%, and that of homozygous + heterozygous-genotype SVs was 6.27%; meanwhile, the proportions were 0.04% and 4.04% when using gamma rays. A higher proportion of SVs were detected when using the carbon ion beam. The gene effects of missense mutations were greater under carbon-ion beam irradiation, and the gene effects of nonsense mutations were greater under gamma-ray irradiation, which meant that the changes in the amino acid sequences were different between the carbon-ion beam and gamma rays. Taken together, our results demonstrate that both carbon-ion beam and gamma rays are effective techniques for rapid mutation breeding in soybean. If one would like to obtain mutations with a low-frequency phenotype, low levels of background genomic mutations and mutations with a higher proportion of SVs, carbon-ion beams are the best choice.https://www.mdpi.com/1422-0067/24/10/8825soybeancarbon-ion beamgamma raysmutation screeningwhole-genome sequencingstructural variation
spellingShingle Zhuo Feng
Yan Du
Jingmin Chen
Xia Chen
Weibin Ren
Lulu Wang
Libin Zhou
Comparison and Characterization of Phenotypic and Genomic Mutations Induced by a Carbon-Ion Beam and Gamma-ray Irradiation in Soybean (<i>Glycine max</i> (L.) Merr.)
International Journal of Molecular Sciences
soybean
carbon-ion beam
gamma rays
mutation screening
whole-genome sequencing
structural variation
title Comparison and Characterization of Phenotypic and Genomic Mutations Induced by a Carbon-Ion Beam and Gamma-ray Irradiation in Soybean (<i>Glycine max</i> (L.) Merr.)
title_full Comparison and Characterization of Phenotypic and Genomic Mutations Induced by a Carbon-Ion Beam and Gamma-ray Irradiation in Soybean (<i>Glycine max</i> (L.) Merr.)
title_fullStr Comparison and Characterization of Phenotypic and Genomic Mutations Induced by a Carbon-Ion Beam and Gamma-ray Irradiation in Soybean (<i>Glycine max</i> (L.) Merr.)
title_full_unstemmed Comparison and Characterization of Phenotypic and Genomic Mutations Induced by a Carbon-Ion Beam and Gamma-ray Irradiation in Soybean (<i>Glycine max</i> (L.) Merr.)
title_short Comparison and Characterization of Phenotypic and Genomic Mutations Induced by a Carbon-Ion Beam and Gamma-ray Irradiation in Soybean (<i>Glycine max</i> (L.) Merr.)
title_sort comparison and characterization of phenotypic and genomic mutations induced by a carbon ion beam and gamma ray irradiation in soybean i glycine max i l merr
topic soybean
carbon-ion beam
gamma rays
mutation screening
whole-genome sequencing
structural variation
url https://www.mdpi.com/1422-0067/24/10/8825
work_keys_str_mv AT zhuofeng comparisonandcharacterizationofphenotypicandgenomicmutationsinducedbyacarbonionbeamandgammarayirradiationinsoybeaniglycinemaxilmerr
AT yandu comparisonandcharacterizationofphenotypicandgenomicmutationsinducedbyacarbonionbeamandgammarayirradiationinsoybeaniglycinemaxilmerr
AT jingminchen comparisonandcharacterizationofphenotypicandgenomicmutationsinducedbyacarbonionbeamandgammarayirradiationinsoybeaniglycinemaxilmerr
AT xiachen comparisonandcharacterizationofphenotypicandgenomicmutationsinducedbyacarbonionbeamandgammarayirradiationinsoybeaniglycinemaxilmerr
AT weibinren comparisonandcharacterizationofphenotypicandgenomicmutationsinducedbyacarbonionbeamandgammarayirradiationinsoybeaniglycinemaxilmerr
AT luluwang comparisonandcharacterizationofphenotypicandgenomicmutationsinducedbyacarbonionbeamandgammarayirradiationinsoybeaniglycinemaxilmerr
AT libinzhou comparisonandcharacterizationofphenotypicandgenomicmutationsinducedbyacarbonionbeamandgammarayirradiationinsoybeaniglycinemaxilmerr