Rapid accumulation of mutations during seed-to-seed propagation of mismatch-repair-defective <i>Arabidopsis</i>

Hoffman, Peter D.; Leonard, Jeffrey M.; Lindberg, Gerrick E.; Bollmann, Stephanie R.; Hays, John B.

doi:10.1101/gad.1217204

Cited by 81 publications

(94 citation statements)

References 21 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…As a result, Frumkin et al (37) needed more markers, as well as mismatch repair-deficient cell lines and plant strains, to detect sufficient somatic diversity. The MSH2-deficient strain of Arabidopsis used by them accumulates mutations throughout the genome and becomes morphologically abnormal (38), making it a somewhat less suitable model of normal development.…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic fate mapping

Salipante¹,

Horwitz

2006

Proc. Natl. Acad. Sci. U.S.A.

111

View full text Add to dashboard Cite

Cell fate maps describe how the sequence of cell division, migration, and apoptosis transform a zygote into an adult. Yet, it is only in Caenorhabditis elegans where microscopic observation of each cell division has allowed for construction of a complete fate map. More complex, and opaque, animals prove less yielding. DNA replication, however, generates somatic mutations. Consequently, multicellular organisms comprise mosaics where most cells acquire unique genomes that are potentially capable of delineating their ancestry. Here we take a phylogenetic approach to passively retrace embryonic relationships by deducing the order in which mutations have arisen during development. We show that polyguanine repeat DNA sequences are particularly useful genetic markers, because they frequently change length during mitosis. To demonstrate feasibility, we phylogenetically reconstruct the lineage of cultured mouse NIH 3T3 cells based on mutations affecting the length of polyguanine markers. We then employ whole genome amplification to genotype polyguanine markers in single cells taken from a mouse and use phylogenetics to infer the developmental relationships of the sampled tissues. The result is consistent with the present understanding of embryogenesis and demonstrates the large scale potential of this method for producing a complete mammalian cell fate at the resolution of a single cell.cell fate ͉ development ͉ genomic instability

show abstract

Section: Discussionmentioning

confidence: 99%

Phylogenetic fate mapping

Salipante¹,

Horwitz

2006

Proc. Natl. Acad. Sci. U.S.A.

111

View full text Add to dashboard Cite

show abstract

“…In the present case, g = 10, the count of identified homozygous mutations is then 10m + 8t/2, which is lower than the expected count of accumulated homozygous mutations, i.e., 10 3 (m + t/2). Although we acknowledge an underestimation of the mutation rate, current knowledge does not permit us to accurately correct it, because the values of m and t are hard to estimate during plant development (Hoffman et al 2004;Ossowski et al 2010). Nevertheless, this underestimation has a limited effect on our results and conclusions because, even in the worst-case scenario, if all mutations originated after the specialization of the reproductive tissues and none originated before the specialization of the reproductive tissues, our current estimation (8t/2) would be 8/10 times the number of true accumulated mutations (10t/2), thus causing a 20% underestimation of the real mutation rate.…”

Section: Calculation Of Mutation Ratementioning

confidence: 99%

“…Taking the average mutation rate of saline transition mutations as an example, n = 42 mutations/9 lines, and g = 10, the mutation rate m = 4.67/10 = 0.467. However, this calculation may be an underestimation of the real mutation rate due to the limited number of generations (Hoffman et al 2004;Ossowski et al 2010), for the following reasons. All new mutations are heterozygous when they arise, and one quarter of the heterozygous mutations present in the germ line before the specialization of the reproductive tissues are expected to be inherited in the homozygous state at the beginning of the next generation (Hoffman et al 2004;Ossowski et al 2010).…”

Section: Calculation Of Mutation Ratementioning

confidence: 99%

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

et al. 2014

View full text Add to dashboard Cite

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

show abstract

“…Therefore, we decided to determine the rate of replication errors in MMR-null plants. MSH2 (MutS protein homolog 2) is an essential MMR component, and previous work with msh2 mutants demonstrated that these plants have a strong mutator phenotype (34).…”

Section: Formation Of De Novo Mutations In Mismatch Repair-deficientmentioning

confidence: 99%

Germline replications and somatic mutation accumulation are independent of vegetative life span inArabidopsis

Watson

Platzer

Kazda

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

In plants, gametogenesis occurs late in development, and somatic mutations can therefore be transmitted to the next generation. Longer periods of growth are believed to result in an increase in the number of cell divisions before gametogenesis, with a concomitant increase in mutations arising due to replication errors. However, there is little experimental evidence addressing how many cell divisions occur before gametogenesis. Here, we measured loss of telomeric DNA and accumulation of replication errors in Arabidopsis with short and long life spans to determine the number of replications in lineages leading to gametes. Surprisingly, the number of cell divisions within the gamete lineage is nearly independent of both life span and vegetative growth. One consequence of the relatively stable number of replications per generation is that older plants may not pass along more somatically acquired mutations to their offspring. We confirmed this hypothesis by genomic sequencing of progeny from young and old plants. This independence can be achieved by hierarchical arrangement of cell divisions in plant meristems where vegetative growth is primarily accomplished by expansion of cells in rapidly dividing meristematic zones, which are only rarely refreshed by occasional divisions of more quiescent cells. We support this model by 5-ethynyl-2′-deoxyuridine retention experiments in shoot and root apical meristems. These results suggest that stem-cell organization has independently evolved in plants and animals to minimize mutations by limiting DNA replication. mutation rate | shoot apical meristem | germline | mismatch repair | telomeres

show abstract

Rapid accumulation of mutations during seed-to-seed propagation of mismatch-repair-defective Arabidopsis

Cited by 81 publications

References 21 publications

Phylogenetic fate mapping

Phylogenetic fate mapping

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

Germline replications and somatic mutation accumulation are independent of vegetative life span inArabidopsis

Contact Info

Product

Resources

About