Regenerant Arabidopsis Lineages Display a Distinct Genome-Wide Spectrum of Mutations Conferring Variant Phenotypes

Jiang, Caifu; Mithani, Aziz; Gan, Xiangchao; Belfield, Eric J.; Klingler, J.; Zhu, Jian‐Kang; Ragoussis, Jiannis; Mott, Richard; Harberd, Nicholas P.

doi:10.1016/j.cub.2011.07.002

Cited by 90 publications

(108 citation statements)

References 37 publications

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“…Finally, mutations that exhibited a heterozygous pattern (e.g., where 20%-80% of reads showed a base different from the reference base) or where there was insufficient coverage in G0 or G10 were also excluded from the final mutation lists. Our previous studies confirmed that ;100% of the mutations detected by the above described multistep variant detection pipeline were real (Jiang et al 2011;Belfield et al 2012). Using this pipeline, we identified 102 and 52 mutations in G10 saline soil and control samples, respectively (Supplemental Tables S2, S3).…”

Section: Salt Content Determinationsupporting

confidence: 58%

“…The transition/transversion (Ti/Tv) ratio of single base substitutions accumulating in A. thaliana MA lineages exposed over multiple successive generations to soilsalinity stress (;1.7) is different from that of control MA lineages (;2.5) (Fig. 1C), but similar to that of mutations accumulated in in vitro regenerant or irradiated A. thaliana lineages (Jiang et al 2011;Belfield et al 2012). Intriguingly, the change in Ti/Tv ratio generated by salt stress in A. thaliana is similar to that generated by the environmental stress response in yeast (Shor et al 2013).…”

Section: Discussionmentioning

confidence: 87%

“…The Col-0 laboratory strain of A. thaliana used in this study was as previously described (Jiang et al 2011). Plants were grown in a long-day (16 h light/8 h dark) photoperiod (light irradiance 120 mmol photons m À2 s…”

Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

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Environmentally responsive genome-wide accumulation of de novoArabidopsis thalianamutations and epimutations

et al. 2014

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Evolution is fueled by phenotypic diversity, which is in turn due to underlying heritable genetic (and potentially epigenetic) variation. While environmental factors are well known to influence the accumulation of novel variation in microorganisms and human cancer cells, the extent to which the natural environment influences the accumulation of novel variation in plants is relatively unknown. Here we use whole-genome and whole-methylome sequencing to test if a specific environmental stress (high-salinity soil) changes the frequency and molecular profile of accumulated mutations and epimutations (changes in cytosine methylation status) in mutation accumulation (MA) lineages of Arabidopsis thaliana. We first show that stressed lineages accumulate~100% more mutations, and that these mutations exhibit a distinctive molecular mutational spectrum (specific increases in relative frequency of transversion and insertion/deletion [indel] mutations). We next show that stressed lineages accumulate~45% more differentially methylated cytosine positions (DMPs) at CG sites (CG-DMPs) than controls, and also show that while many (~75%) of these CG-DMPs are inherited, some can be lost in subsequent generations. Finally, we show that stress-associated CG-DMPs arise more frequently in genic than in nongenic regions of the genome. We suggest that commonly encountered natural environmental stresses can accelerate the accumulation and change the profiles of novel inherited variants in plants. Our findings are significant because stress exposure is common among plants in the wild, and they suggest that environmental factors may significantly alter the rates and patterns of incidence of the inherited novel variants that fuel plant evolution.[Supplemental material is available for this article.]In The Origin of Species, Darwin identified heritable variation as fundamental to biological evolution (Darwin 1859), although he could not define that variation. We now understand that the heritable variation underlying evolution is substantially due to genetic (e.g., DNA sequence mutation) and potentially to epigenetic (e.g., altered cytosine methylation or histone modification status) change

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Section: Salt Content Determinationsupporting

confidence: 58%

Section: Discussionmentioning

confidence: 87%

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Environmentally responsive genome-wide accumulation of de novoArabidopsis thalianamutations and epimutations

et al. 2014

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“…1d) appear to be in the middle between those reported for spontaneous mutations (2.41-2.73 (Ossowski et al, 2010)) and fast-neutron-induced mutations (0.86 (Belfield et al, 2012)) in Arabidopsis plants. The Ti/Tv ratios are slightly lower than those reported for ethylmethane sulfonate (EMS) mutagenesis (1.63-1.83 (MohdYusoff et al, 2015)) and greater than those in regenerated plants of rice (1.1 (Miyao et al, 2012)) and Arabidopsis (0.92 (Jiang et al, 2011)). These differences must be related to the nature of mutagens, but the underlying mechanism awaits further study.…”

Section: Type Of γ Irradiation-induced Mutationsmentioning

confidence: 60%

Frequency and type of inheritable mutations induced by γ rays in rice as revealed by whole genome sequencing

Zheng

Hairui

et al. 2016

J. Zhejiang Univ. Sci. B

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Mutation breeding is based on the induction of genetic variations; hence knowledge of the frequency and type of induced mutations is of paramount importance for the design and implementation of a mutation breeding program. Although γ ray irradiation has been widely used since the 1960s in the breeding of about 200 economically important plant species, molecular elucidation of its genetic effects has so far been achieved largely by analysis of target genes or genomic regions. In the present study, the whole genomes of six γ-irradiated M 2 rice plants were sequenced; a total of 144-188 million high-quality (Q>20) reads were generated for each M 2 plant, resulting in genome coverage of >45 times for each plant. Single base substitution (SBS) and short insertion/deletion (Indel) mutations were detected at the average frequency of 7.5×10 −6 -9.8×10 −6 in the six M 2 rice plants (SBS being about 4 times more frequent than Indels). Structural and copy number variations, though less frequent than SBS and Indel, were also identified and validated. The mutations were scattered in all genomic regions across 12 rice chromosomes without apparent hotspots. The present study is the first genome-wide single-nucleotide resolution study on the feature and frequency of γ irradiation-induced mutations in a seed propagated crop; the findings are of practical importance for mutation breeding of rice and other crop species.

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“…These procedures produced regenerated plants (R1), and the next generation phase (R2) was obtained from seeds that were collected from the R1 regenerants. The pH of all media was adjusted to 5.8 and autoclaved at 121°C for 20 min (Jiang et al 2011). Control plants were grown on a hormone-free MS medium in the same conditions as the plants used as the source of explants.…”

Section: Plant Materials and In Vitro Culturementioning

confidence: 99%

Chromosome variations in regenerants of Arabidopsis thaliana derived from 2- and 6-week-old callus detected using flow cytometry and FISH analyses

Orzechowska

Stępień

Kamińska

et al. 2012

Plant Cell Tiss Organ Cult

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Shoot organogenesis was induced from 2-and 6-week-old callus derived from the leaves of Arabidopsis thaliana ecotype Columbia (2n = 10). Regenerated plants were evaluated for chromosomal variations by means of flow cytometry and fluorescent in situ hybridization (FISH). Flow cytometric measurements revealed the occurrence of diploid, tetraploid, and octoploid plants among the regenerants of 2-week-old calli, whereas only diploid and tetraploid plants were regenerated from the 6-week-old calli. Chromosome counting showed that plants developed from the 2-week-old calli exhibited mixoploidy and a high frequency of aneuploid cells. These plants were infertile and displayed altered morphology. FISH with 5S and 25S rDNA probes allowed to detect some structural chromosomal rearrangements in regenerated plants. Along with cells which exhibited correct localisation of rDNA loci, also cells bearing chromosomal translocations, deletions or duplications were found. The type of structural aberrations varied between diploid and tetraploid regenerants.

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Regenerant Arabidopsis Lineages Display a Distinct Genome-Wide Spectrum of Mutations Conferring Variant Phenotypes

Cited by 90 publications

References 37 publications

Environmentally responsive genome-wide accumulation of de novoArabidopsis thalianamutations and epimutations

Environmentally responsive genome-wide accumulation of de novoArabidopsis thalianamutations and epimutations

Frequency and type of inheritable mutations induced by γ rays in rice as revealed by whole genome sequencing

Chromosome variations in regenerants of Arabidopsis thaliana derived from 2- and 6-week-old callus detected using flow cytometry and FISH analyses

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