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By sequencing 60 samples at high-coverage, we explore the within individual-variation (de novo mutations) of two tropical trees with branches exposed to high and low light. We explore: (1) their frequencies, (2) their transmissions, and their distribution (3) with branch topology, and (4) in response to UVs.

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Given that the quality of the reference genomes are known to be crucial to ensure accurate de novo mutation detection, we used a combination of high-fidelity reads and optical maps to generate near chromosome-level assembly for the 2 tree species.

Here is an example for Dicorynia guianensis.

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Using a method initially developed for cancer and then adapted to plants, we identified >18k somatic mutations. <10% are restricted to a single branch and >40% originate from the base of the crown, with no fit between branching topology and the mutation phylogenies, challenging current expectations regarding somatic mutations in plants.

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We found no difference in the number of mutations, the type of mutations (nucleotide changes), or the mutation spectra (the mutation context, including the bases immediately 5' and 3') between the branches exposed to high vs. low light conditions!!

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Combined with a reanalysis of other tree species, we observe that all have very few mutations at high frequency. Low-frequency mutations account for the vast majority of within-individual somatic diversity in plants (>90% with f<0.25).

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Emphasising the importance of allelic fraction (AF), we found that the average AF in non-synonymous sites was lower than in syn. sites, consistent with intra-organismal purifying selection of non-synonymous mutations. Somatic mutations are therefore more deleterious than adaptive

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Low-frequency somatic mutations are not only more numerous within the plant, they are also transmitted, and therefore have an evolutionary future! Among the mutations tested, we demonstrated the transmission of ~10% of mutations to embryos. All were at low frequency in the crown!

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Low-frequency somatic mutations are thus heritable and contribute to within-species standing genetic variation, the fuel of evolution, challenging current tacit assumptions that only high-frequency mutations would matter for evolution.

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Our results are consistent with far more complex links between growth, ageing and heritable mutation rates than commonly thought in plants, along the lines of recent empirical evidence in animals (Cagan et al. 2022, Bergeron et al. 2023).

We call for a new view on somatic mutations in plants with renewed assumptions: (i) the distribution of mutations does not necessarily correspond to the branching topology, (ii) most somatic mutations are at low-frequency and (iii) can be transmitted.

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