Physiological status of plant tissue affects the frequency and types of mutations induced by carbon-ion irradiation in Arabidopsis

Hase, Yoshihiro; Satoh, Katsuya; Kitamura, Satoshi; Oono, Yutaka

doi:10.1038/s41598-018-19278-1

Cited by 48 publications

(81 citation statements)

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“…The average number of mutated genes, including both homozygous and heterozygous mutations, was 13 in each M 3 mutant (Kazama et al ., ; Du et al ., ). In the case of randomly chosen M 2 lines, an average of 7.0 genes were affected as homozygous mutations (Hase et al ., ). In addition, relatively large deletions and genomic rearrangements, such as inversions and translocations, were also detected by WGS of selected carbon‐ion irradiation‐derived mutants.…”

Section: Introductionmentioning

confidence: 97%

Targeted exome sequencing of unselected heavy‐ion beam‐irradiated populations reveals less‐biased mutation characteristics in the rice genome

et al. 2019

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SummaryHeavy‐ion beams have been widely utilized as a novel and effective mutagen for mutation breeding in diverse plant species, but the induced mutation spectrum is not fully understood at the genome scale. We describe the development of a multiplexed and cost‐efficient whole‐exome sequencing procedure in rice, and its application to characterize an unselected population of heavy‐ion beam‐induced mutations. The bioinformatics pipeline identified single‐nucleotide mutations as well as small and large (>63 kb) insertions and deletions, and showed good agreement with the results obtained with conventional polymerase chain reaction (PCR) and sequencing analyses. We applied the procedure to analyze the mutation spectrum induced by heavy‐ion beams at the population level. In total, 165 individual M2 lines derived from six irradiation conditions as well as eight pools from non‐irradiated ‘Nipponbare’ controls were sequenced using the newly established target exome sequencing procedure. The characteristics and distribution of carbon‐ion beam‐induced mutations were analyzed in the absence of bias introduced by visual mutant selections. The average (±SE) number of mutations within the target exon regions was 9.06 ± 0.37 induced by 150 Gy irradiation of dry seeds. The mutation frequency changed in parallel to the irradiation dose when dry seeds were irradiated. The total number of mutations detected by sequencing unselected M2 lines was correlated with the conventional mutation frequency determined by the occurrence of morphological mutants. Therefore, mutation frequency may be a good indicator for sequencing‐based determination of the optimal irradiation condition for induction of mutations.

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Section: Introductionmentioning

confidence: 97%

Targeted exome sequencing of unselected heavy‐ion beam‐irradiated populations reveals less‐biased mutation characteristics in the rice genome

et al. 2019

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“…The characterization of the molecular nature of mutations is important for the efficient use of different types of mutagen treatments. Recent advances in high-throughput sequencing technologies have greatly accelerated the understanding of the molecular nature of mutations, particularly those induced by high-LET radiation (Belfield et al, 2012;Hirano et al, 2015;Du et al, 2017;Kazama et al, 2017;Hase et al, 2018;Ichida et al, 2019;Jo and Kim, 2019). An extensive analysis in Arabidopsis suggested that ion beams with very high LET values induce drastic and complex alterations of chromosomes, while ion beams with moderate LET values often induce short insertions and deletions (InDels).…”

Section: Introductionmentioning

confidence: 99%

“…Thus, the use of the latter is preferable to achieve a high frequency of loss-of-function mutations (Kazama et al, 2017). We previously compared the mutations induced by carbon ion irradiation of Arabidopsis dry seeds and seedlings, and we demonstrated that the tissue type greatly affected the frequency and types of mutations (Hase et al, 2018). A neutron is also a kind of high-LET radiation, and a large-scale mutant population having a mutation database determined by whole-genome resequencing was constructed in the model rice cultivar Kitaake (Li et al, 2016.…”

Section: Introductionmentioning

confidence: 99%

“…For the chronic gamma irradiation, mutation accumulation lines were prepared by recurrent irradiation over five successive generations to evaluate accurately the mutations induced even at low dose rates. The results were compared with the data for carbon ion irradiation obtained in our previous study (Hase et al, 2018) to elucidate how many and what types of mutations are induced and how many genes are affected in a genome by acute/chronic gamma and carbon ion irradiation.…”

Section: Introductionmentioning

confidence: 99%

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Genetic Consequences of Acute/Chronic Gamma and Carbon Ion Irradiation of Arabidopsis thaliana

et al. 2020

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Gamma rays are the most frequently used ionizing radiation in plant mutagenesis; however, few studies are available on the characteristics of mutations at a genome-wide level. Here, we quantitatively and qualitatively characterized the mutations induced by acute/chronic gamma ray irradiation in Arabidopsis. The data were then compared with those previously obtained for carbon ion irradiation. In the acute irradiation of dry seeds at the same effective survival dose, gamma rays and carbon ions differed substantially, with the former inducing a significantly greater number of total mutation events, while the number of gene-affecting mutation events did not differ between the treatments. This may result from the gamma rays predominantly inducing single-base substitutions, while carbon ions frequently induced deletions ≥2 bp. Mutation accumulation lines prepared by chronic gamma irradiation with 100-500 mGy/h in five successive generations showed higher mutation frequencies per dose compared with acute irradiation of dry seeds. Chronic gamma ray irradiation may induce larger genetic changes compared with acute gamma ray irradiation. In addition, the transition/transversion ratio decreased as the dose rate increased, suggesting that plants responded to very low dose rates of gamma rays (∼1 mGy/h), even though the overall mutation frequency did not increase. These data will aid our understanding of the effects of radiation types and be useful in selecting suitable radiation treatments for mutagenesis.

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“…A similar trend was observed in the presence of homopolymers or polynucleotide repeats at flanking sequences of small InDels in the genome of carbon ion-beam-irradiated Arabidopsis [18,20]. Hase et al [34] inferred that distinct mechanisms are involved in between the generation of the single base deletion and larger-sized deletions in carbon ion-irradiated Arabidopsis. They also suggested that much larger size deletions (≧ 50 bp) are generated via another distinct mechanism.…”

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confidence: 62%

Genome sequencing of ion-beam-induced mutants facilitates detection of candidate genes responsible for phenotypes of mutants in rice

Oono

Ichida

Morita

et al. 2019

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30Ion beams are physical mutagens and used for plant and microbe breeding. They 31 are thought to cause mutations via a distinct mechanism from chemical mutagens or 32 gamma rays. Characteristics of ion-beam-induced mutations have been analyzed using 33 marker genes; however, little is known about the extent of the mutations induced by ion 34 beams at a genomic level. To understand the properties of ion beam-induced mutations at 35 a genomic level, we conducted whole-exome sequencing of rice DNA. DNA extracted 36 from carbon-ion-beam-induced rice mutants were fragmented and captured with a custom 37 probe library covering 66.3 M bases of all exons and miRNAs. A total of 56 mutations, 38 including 24 single nucleotide variations, 23 deletions, and 5 insertions, were detected in 39 5 mutant rice lines (2 dwarf and 3 early-heading-date mutants). The mutations were 40 distributed among all 12 chromosomes, and the average mutation frequency in the M1 41 generation was estimated to be 2.6 × 10 -7 per base. Many single base insertions and 42 deletions were associated with homopolymeric repeats, whereas larger deletions up to 7 43 base pairs were more linked to polynucleotide repeats in the DNA sequences of the 44 mutation sites. Among 56 mutations, 6 (1.2 mutations per line on average) were classified 45 as high-impact mutations that caused a frame shift or loss of exons. A gene that was 46 functionally related to the phenotype of the mutant was disrupted by a high-impact 47 mutation in 4 of the 5 lines, suggesting that whole-exome sequencing of an ion-beam-48 irradiated mutant could facilitate detection of a candidate gene responsible for the mutant 49 phenotype. 50 3 51 Introduction 52 Ion beams are charged particles that are derived from particle accelerators using 53 electromagnetic fields. As with other ionizing radiations, ion beams cause damage to 54 DNA molecules in living organisms and have been used as physical mutagens for plant 55 and microbe breeding [1-3]. Ion beams are characterized by the deposition of a high 56 energy transfer per unit length (linear energy transfer, LET) and are believed to induce 57 mutations as a consequence of distinct biological effects from low LET radiation such as 58 gamma-rays and electrons. In fact, during the screening of mutants from irradiated 59 explants of carnations, ion beams induced a wider variety of mutants in terms of flower 60 color and shape than gamma-rays and X-rays [4]. The appearance of more flower color 61 variations in the ion-beam-irradiated population has also been observed in 62 chrysanthemums [1]. In contrast, no remarkable difference in the mutation spectrum 63between ion-beam and gamma-ray irradiation has also been observed [5]. 64Characterization of ion beam-induced mutations in plant DNA was conducted via 65 several approaches using Arabidopsis, a model plant for plant molecular genetics. The 66 most common approach for characterizing germline mutations is the isolation of mutants 67 deficient in well-characterized marker genes responsible for visibl...

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Physiological status of plant tissue affects the frequency and types of mutations induced by carbon-ion irradiation in Arabidopsis

Cited by 48 publications

References 24 publications

Targeted exome sequencing of unselected heavy‐ion beam‐irradiated populations reveals less‐biased mutation characteristics in the rice genome

Targeted exome sequencing of unselected heavy‐ion beam‐irradiated populations reveals less‐biased mutation characteristics in the rice genome

Genetic Consequences of Acute/Chronic Gamma and Carbon Ion Irradiation of Arabidopsis thaliana

Genome sequencing of ion-beam-induced mutants facilitates detection of candidate genes responsible for phenotypes of mutants in rice

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