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An organism becomes genetically mosaic through the accumulation of somatic mutations. Genetic mosaicism is a commonality of multicellular life and has been studied extensively in humans due to its associations with aging and diseases. In humans, somatic selection shapes the accumulation of somatic mutations, with strong signatures of positive somatic selection in cancer cell lineages. So far, evidence for somatic selection in plants has been inconsistent. The evolutionary implications of genetic mosaicism in humans and other animals are limited by early specification of germline cells, preventing transmission of somatic mutations to progeny. In contrast, many plant lineages reproduce asexually with clonal progeny derived from vegetative tissues. We describe the patterns and processes shaping somatic mutation accumulation within a single, 149-year-old historic sweet orange (Citrus sinensis) tree and within a clonal lineage of sweet orange. More than 12,000 somatic mutations were identified in the historic tree and 28,000 somatic mutations were identified across 199 clonally related sweet orange accessions. Both the spatial and genomic distributions of somatic mutations are non-random. The spatial patterns of somatic mutations across the historic tree depend on tree growth and development and their accumulation across the tree canopy recapitulates branching topology. Analysis of the genomic distribution of somatic mutations revealed that the subtelomeres, which are large arrays of ~180 bp repeats, are mutation hotspots. Finally, there was genomic evidence that somatic selection shapes the accumulation of somatic mutations both within the historic tree and also during clonal propagation.
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Mosaic of Somatic Mutations in Earth’s Oldest Living Organism, Pando
Understanding how mutations arise and spread through individuals and populations is fundamental to evolutionary biology. Most organisms have a life cycle with unicellular bottlenecks during reproduction. However, some organisms like plants, fungi, or colonial animals can grow indefinitely, changing the manner in which mutations spread throughout both the individual and the population. Furthermore, clonally reproducing organisms may also achieve exceedingly long lifespans, making somatic mutation an important mechanism of creating heritable variation for Darwinian evolution by natural selection. Yet, little is known about intra-organism mutation rates and evolutionary trajectories in long-lived species. Here, we study the Pando aspen clone, the largest known quaking aspen (Populus tremuloides) clone founded by a single seedling and thought to be one of the oldest studied organisms. Aspen reproduce vegetatively via new root-borne stems forming clonal patches, sometimes spanning several hectares. To study the evolutionary history of the Pando clone, we collected and sequenced over 500 samples from Pando and neighboring clones, as well as from various tissue types within Pando, including leaves, roots, and bark. We applied a series of filters to distinguish somatic mutations from the pool of both somatic and germline mutations, incorporating a technical replicate sequencing approach to account for uncertainty in somatic mutation detection. Despite root spreading being spatially constrained, we observed only a modest positive correlation between genetic and spatial distance, suggesting the presence of a mechanism preventing the accumulation and spread of mutations across units. Phylogenetic models estimate the age of the clone to between ~16,000-80,000 years. This age is generally corroborated by the near-continuous presence of aspen pollen in a lake sediment record collected from Fish Lake near Pando. Overall, this work enhances understanding of mutation accumulation and dispersal within and between ramets of long-lived, clonally-reproducing organisms. Significance StatementThis study enhances our understanding of evolutionary processes in long-lived clonal organisms by investigating somatic mutation accumulation and dispersal patterns within the iconic Pando aspen clone. The authors estimated the clone to be between 10,000 and 80,000 years old and uncovered a modest spatial genetic structure in the 42.6-hectare clone, suggesting localized mutation build-up rather than dispersal along tissue lineages. This work sheds light on an ancient organism and how plants may evolve to preserve genetic integrity in meristems fueling indefinite growth, with implications for our comprehension of adaptive strategies in long-lived perennials.
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- Award ID(s):
- 1845363
- PAR ID:
- 10584991
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
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- Posted Content:
- https://doi.org/10.1101/2024.10.19.619233
