The vast majority of somatic mutations in plants are layer-specific

Goel, Manish; Campoy, Jose A.; Krause, Kristin; Baus, Lisa C.; Sahu, Anshupa; Sun, Hequan; Walkemeier, Birgit; Marek, Magdalena; Beaudry, Randy; Ruiz, David; Huettel, Bruno; Schneeberger, Korbinian

doi:10.1101/2024.01.04.573414

Cited by 3 publications

(2 citation statements)

References 86 publications

(102 reference statements)

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“…The latter are complicated due to stem cell stratification into layers 28 . However, even under these circumstances, the somatic genetic clock can be applied when either the sampled tissue is dominated by one meristematic layer (as is the case in eelgrass Z. marina) or when descendant tissues of a certain stem cell population can be clearly distinguished among the adult plant organs 31 .…”

Section: Discussionmentioning

confidence: 99%

“…We thus continued by simplifying the fixation dynamics by assuming a one-layer case, enabling the application of our model of a generic clonal organism to eelgrass. However, assuming that cell growth and division frequency is similar across layers 30 , the model can be applied to any cell layer and derived organs in stratified meristems 31 . We parametrized the model for eelgrass and focused on the most likely range with N = 7-12 and N 0 = 3-4 (Fig.…”

Section: Application Of the Somatic Genetic Clock In A Seagrassmentioning

confidence: 99%

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A somatic genetic clock for clonal species

Yu,

Renton,

Burian

et al. 2024

Nat Ecol Evol

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Age and longevity are key parameters for demography and life-history evolution of organisms. In clonal species, a widespread life history among animals, plants, macroalgae and fungi, the sexually produced offspring (genet) grows indeterminately by producing iterative modules, or ramets, and so obscure their age. Here we present a novel molecular clock based on the accumulation of fixed somatic genetic variation that segregates among ramets. Using a stochastic model, we demonstrate that the accumulation of fixed somatic genetic variation will approach linearity after a lag phase, and is determined by the mitotic mutation rate, without direct dependence on asexual generation time. The lag phase decreased with lower stem cell population size, number of founder cells for the formation of new modules, and the ratio of symmetric versus asymmetric cell divisions. We calibrated the somatic genetic clock on cultivated eelgrass Zostera marina genets (4 and 17 years respectively). In a global data set of 20 eelgrass populations, genet ages were up to 1,403 years. The somatic genetic clock is applicable to any multicellular clonal species where the number of founder cells is small, opening novel research avenues to study longevity and, hence, demography and population dynamics of clonal species.

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Section: Discussionmentioning

confidence: 99%

Section: Application Of the Somatic Genetic Clock In A Seagrassmentioning

confidence: 99%

A somatic genetic clock for clonal species

Yu,

Renton,

Burian

et al. 2024

Nat Ecol Evol

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Investigating low frequency somatic mutations inArabidopsiswith Duplex Sequencing

Waneka,

Pate,

Monroe

et al. 2024

Preprint

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Mutations are the source of novel genetic diversity but can also lead to disease and maladaptation. The conventional view is that mutations occur randomly with respect to their environment-specific fitness consequences. However, intragenomic mutation rates can vary dramatically due to transcription coupled repair and based on local epigenomic modifications, which are non-uniformly distributed across genomes. One sequence feature associated with decreased mutation is higher expression level, which can vary depending on environmental cues. To understand whether the association between expression level and mutation rate creates a systematic relationship with environment-specific fitness effects, we perturbed expression through a heat treatment inArabidopsis thaliana. We quantified gene expression to identify differentially expressed genes, which we then targeted for mutation detection using Duplex Sequencing. This approach provided a highly accurate measurement of the frequency of rare somatic mutations in vegetative plant tissues, which has been a recent source of uncertainty in plant mutation research. We included mutant lines lacking mismatch repair (MMR) and base excision repair (BER) capabilities to understand how repair mechanisms may drive biased mutation accumulation. We found wild type (WT) and BER mutant mutation frequencies to be very low (mean variant frequency 1.8×10-8and 2.6×10-8, respectively), while MMR mutant frequencies were significantly elevated (1.13×10-6). These results show that somatic variant frequencies are extremely low in WT plants, indicating that larger datasets will be needed to address the fundamental evolutionary question as to whether environmental change leads to gene-specific changes in mutation rate.SIGNIFICANCEAccurately measuring mutations in plants grown under different environments is important for understanding the determinants of mutation rate variation across a genome. Given the low rate ofde novomutation in plant germlines, such measurements can take years to obtain, hindering tests of mutation accumulation under varying environmental conditions. We implemented highly accurate Duplex Sequencing to study somatic mutations in plants grown in two different temperatures. In contrast to plants with deficiencies in DNA mismatch repair machinery, we found extremely low mutation frequencies in wild type plants. These findings help resolve recent uncertainties about the somatic mutation rate in plant tissues and indicate that larger datasets will be necessary to understand the interaction between mutation and environment in plant genomes.

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The vast majority of somatic mutations in plants are layer-specific

Goel,

Campoy,

Krause

et al. 2024

Genome Biol

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Background Plant meristems are structured organs consisting of distinct layers of stem cells, which differentiate into new plant tissue. Mutations in meristematic layers can propagate into large sectors of the plant. However, the characteristics of meristematic mutations remain unclear, limiting our understanding of the genetic basis of somaclonal phenotypic variation. Results Here, we analyse the frequency and distribution of somatic mutations in an apricot tree. We separately sequence the epidermis (developing from meristem layer 1) and the flesh (developing from meristem layer 2) of several fruits sampled across the entire tree. We find that most somatic mutations (> 90%) are specific to individual layers. Interestingly, layer 1 shows a higher mutation load than layer 2, implying different mutational dynamics between the layers. The distribution of somatic mutations follows the branching of the tree. This suggests that somatic mutations are propagated to developing branches through axillary meristems. In turn, this leads us to the unexpected observation that the genomes of layer 1 of distant branches are more similar to each other than to the genomes of layer 2 of the same branches. Finally, using single-cell RNA sequencing, we demonstrate that layer-specific mutations were only transcribed in the cells of the respective layers and can form the genetic basis of somaclonal phenotypic variation. Conclusions Here, we analyse the frequency and distribution of somatic mutations with meristematic origin. Our observations on the layer specificity of somatic mutations outline how they are distributed, how they propagate, and how they can impact clonally propagated crops.

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The vast majority of somatic mutations in plants are layer-specific

Cited by 3 publications

References 86 publications

A somatic genetic clock for clonal species

A somatic genetic clock for clonal species

Investigating low frequency somatic mutations inArabidopsiswith Duplex Sequencing

The vast majority of somatic mutations in plants are layer-specific

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