Plant mutations: slaying beautiful hypotheses by surprising evidence

Somatic mutations potentially play a role in plant evolution, but common expectations pertaining to plant somatic mutations remain insufficiently tested. Unlike in most animals, the plant germline is assumed to be set aside late in development, leading to the expectation that plants accumulate somatic mutations along growth. Therefore, several predictions were made on the fate of somatic mutations: mutations have generally low frequency in plant tissues; mutations at high frequency have a higher chance of intergenerational transmission; branching topology of the tree dictates mutation distribution; and, exposure to UV radiation increases mutagenesis. To provide new insights into mutation accumulation and transmission in plants, we produced two high-quality reference genomes and a unique dataset of 60 high-coverage whole-genome sequences of two tropical tree species, Dicorynia guianensis (Fabaceae) and Sextonia rubra (Lauraceae). We identified 15,066 de novo somatic mutations in D. guianensis and 3,208 in S. rubra, surprisingly almost all found at low frequency. We demonstrate that: 1) low-frequency mutations can be transmitted to the next generation; 2) mutation phylogenies deviate from the branching topology of the tree; and 3) mutation rates and mutation spectra are not demonstrably affected by differences in UV exposure. Altogether, our results suggest far more complex links between plant growth, ageing, UV exposure, and mutation rates than commonly thought. Significance StatementThe origin and fate of new mutations have received less attention in plants than in animals. Similarly to animals, plant mutations are expected to accumulate with growth and time, and under exposure to UV light. However, contrary to animals, plant reproductive organs form late in an individuals development, allowing the transmission to the progeny of mutations accumulated along growth. Here, we resequenced DNA from different branches differentially exposed to sunlight of two tropical tree species. We showed that new mutations are generally rare in plant tissues and do not mimic branching patterns but can nevertheless be transmitted to the progeny. Our findings provide a new perspective on heritable plant mutation and its pivotal role as the engine of evolution.