Causes of Mutation Rate Variability in Plant Genomes

Quiroz, Daniela; Lensink, Mariele; Kliebenstein, Daniel J.; Monroe, J. Grey

doi:10.1146/annurev-arplant-070522-054109

Cited by 14 publications

(8 citation statements)

References 152 publications

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“…2018; Monroe et al . 2022; Quiroz et al . 2023), as is the fact that gene expression is environmentally determined (Richards et al .…”

Section: Discussionmentioning

confidence: 99%

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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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“…2018; Monroe et al . 2022; Quiroz et al . 2023), as is the fact that gene expression is environmentally determined (Richards et al .…”

Section: Discussionmentioning

confidence: 99%

“…2019) and in introns compared to exons (Monroe et al . 2022, 2023a; Quiroz et al . 2023; Staunton et al .…”

Section: Introductionmentioning

confidence: 99%

Investigating low frequency somatic mutations inArabidopsiswith Duplex Sequencing

Waneka,

Pate,

Monroe

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

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“…Genetic drift is more profound in chloroplast DNA compared to the nuclear genome, which could explain the difference observed between the two marker systems. Increased mutation rates, weaker force of genetic drift and migration in nuclear DNA of polyploids also leads to a better evening out of the allele frequencies compared to haploid plastid loci (Quiroz et al, 2023).…”

Section: Discussionmentioning

confidence: 99%

Genetic monitoring for effective plant conservation: An example using the threatened Saxifraga hirculus L. in Scotland

Finger,

Macdonald,

Hollingsworth

2023

Plants People Planet

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Societal Impact StatementMany mountain plants persist in small, isolated patches on the verge of extinction. Observational methods of monitoring these populations, such as recording the number of flowering stems, do not indicate the number of genetically distinct individuals, which is crucial information for conserving small populations. Here, the rate of clonal reproduction and number of genetic individuals were measured in the threatened Saxifraga hirculus in Scotland. These methods showed that population size is a poor proxy for genotype diversity and identified highly diverse small populations that may otherwise have been overlooked. This highlights the necessity of using genetic data to ensure the successful conservation of threatened plants.Summary Habitat fragmentation and loss increase the isolation of plant populations, increasing the occurrence of within population reproduction, and the potential for negative genetic effects, such as inbreeding depression and loss of genetic diversity. We use the European protected Marsh Saxifrage (Saxifraga hirculus) in Scotland as an example for declining perennial plants and the genetic resources they encapsulate. S. hirculus has declined due to agricultural intensification, drainage, industrial afforestation and grazing. The species can spread by seed or vegetatively through the production of rhizomes. Flowering is rare though due to grazing, which limits sexual reproduction and gene flow. An almost complete genetic inventory of Scottish populations was done using 11 microsatellite markers. Furthermore, archived DNA samples were used to document temporal genetic changes. We showed that clonal growth is predominant in some populations and genetic diversity (HS and allelic richness) is relatively high. However, the number of genetically distinct individuals (genets) per population is extremely low (3–34). Archived DNA samples showed that some populations consist of the same few genets with no evidence for turnover. Thus, while clonal growth may have helped the species to persist, there is limited creation of new gene combinations. Our findings highlight that reducing grazing pressure and increasing gene flow will be essential to rescue this species from its evolutionary dead end. We demonstrate the benefits of genetic monitoring for determining census population sizes and thus effective plant management and conservation. This work further sets out a strategy for moving this species towards demographic and genetic sustainability.

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“…Enhanced host plant resistance-and, more importantly, the combination of several effective Lr genes-remains the most feasible, economical, and environmentally friendly approach to ensuring durable resistance [70][71][72][73]. Wheat cultivars and breeding lines with multiple Lr-resistant genes have significantly lower disease levels [74,75], and the use of this kind of resistance has the potential to significantly reduce disease epidemics. A significant number of the Lr genes are race-specific and generally conform to the "gene-for-gene" model proposed by Flor [76], conferring resistance to pathogen races with corresponding Avr genes.…”

Section: Markersmentioning

confidence: 99%

“…The stacking (or pyramiding) of multiple resistance genes is necessary to prolong resistance durability and enhance the effective use of Lr genes [1]. The Lr locus Lr1 was mapped at the 5D [75,76], 5DL [77] chromosome of bread wheat and has been shown to likely continue to play a role in gene combination; it is also highly effective against avirulent pathotypes. This gene was also isolated so that the sequence could be used to validate the linkage to our markers used in this study (Table 2).…”

Section: Genotyping With Kasp Markers and Comparison With Phenotyping...mentioning

confidence: 99%

Phenotyping and Exploitation of Kompetitive Allele-Specific PCR Assays for Genes Underpinning Leaf Rust Resistance in New Spring Wheat Mutant Lines

Kenzhebayeva,

Mazkirat,

Shoinbekova

et al. 2024

CIMB

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Leaf rust (Puccinia triticina Eriks) is a wheat disease causing substantial yield losses in wheat production globally. The identification of genetic resources with permanently effective resistance genes and the generation of mutant lines showing increased levels of resistance allow the efficient incorporation of these target genes into germplasm pools by marker-assisted breeding. In this study, new mutant (M3 generation) lines generated from the rust-resistant variety Kazakhstanskaya-19 were developed using gamma-induced mutagenesis through 300-, 350-, and 400-Gy doses. In field trials after leaf rust inoculation, 75 mutant lines showed adult plant resistance. These lines were evaluated for resistance at the seedling stage via microscopy in greenhouse experiments. Most of these lines (89.33%) were characterized as resistant at both developmental stages. Hyperspectral imaging analysis indicated that infected leaves of wheat genotypes showed increased relative reflectance in visible and near-infrared light compared to the non-infected genotypes, with peak means at 462 and 644 nm, and 1936 and 2392 nm, respectively. Five spectral indexes, including red edge normalized difference vegetation index (RNDVI), structure-insensitive pigment index (SIPI), ratio vegetation index (RVSI), water index (WI), and normalized difference water index (NDWI), demonstrated significant potential for determining disease severity at the seedling stage. The most significant differences in reflectance between susceptible and resistant mutant lines appeared at 694.57 and 987.51 nm. The mutant lines developed were also used for the development and validation of KASP markers for leaf rust resistance genes Lr1, Lr2a, Lr3, Lr9, Lr10, and Lr17. The mutant lines had high frequencies of “a” resistance alleles (0.88) in all six Lr genes, which were significantly associated with seedling resistance and suggest the potential of favorable haplotype introgression through functional markers. Nine mutant lines characterized by the presence of “b” alleles in Lr9 and Lr10—except for one line with allele “a” in Lr9 and three mutant lines with allele “a” in Lr10—showed the progressive development of fungal haustorial mother cells 72 h after inoculation. One line from 300-Gy-dosed mutant germplasm with “b” alleles in Lr1, Lr2a, Lr10, and Lr17 and “a” alleles in Lr3 and Lr9 was characterized as resistant based on the low number of haustorial mother cells, suggesting the contribution of the “a” alleles of Lr3 and Lr9.

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Causes of Mutation Rate Variability in Plant Genomes

Cited by 14 publications

References 152 publications

Investigating low frequency somatic mutations inArabidopsiswith Duplex Sequencing

Investigating low frequency somatic mutations inArabidopsiswith Duplex Sequencing

Genetic monitoring for effective plant conservation: An example using the threatened Saxifraga hirculus L. in Scotland

Phenotyping and Exploitation of Kompetitive Allele-Specific PCR Assays for Genes Underpinning Leaf Rust Resistance in New Spring Wheat Mutant Lines

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